JSLHR
Supplement
Characteristics of Vocal Fold Vibrations in Vocally Healthy Subjects: Analysis With Multi-Line Kymography Akihito Yamauchi,a Hiroshi Imagawa,a Ken-Ichi Sakakibara,b Hisayuki Yokonishi,a Takaharu Nito,a Tatsuya Yamasoba,a and Niro Tayamac
Purpose: In this study, the authors aimed to analyze longitudinal data from high-speed digital images in normative subjects using multi-line kymography. Method: Vocally healthy subjects were divided into young (9 men and 17 women; Mage = 27 years) and older groups (8 men and 12 women; Mage = 73 years). From high-speed digital images of phonation at a conversational frequency kymograms were created at 5 different levels of the vocal fold and were analyzed to determine the opening/closing longitudinal phase difference, open quotient, and speed index. Then age- and gender-related differences of these parameters were analyzed statistically. Results: Young women frequently showed a pattern of posterior-to-anterior glottal opening and anterior-to-posterior
V
ideostroboscopy is widely used for the observation of vocal fold vibrations (Deliyski & Hillman, 2010; Verikas, Uloza, Bacauskiene, Gelzinis, & Kelertas, 2009). However, preceding periodic phonation with a stable fundamental frequency is needed for the production of videostroboscopic oscillating images, which means that videostroboscopy is not applicable to unstable phonation, such as transient, subharmonic, or aperiodic phonation. For the observation of such unstable vocal fold dynamics, highspeed digital imaging (HSDI) is considered more suitable (Kendall, 2009; Olthoff, Woywod, & Kruse, 2007; Patel, Dailey, & Bless, 2008). Because it can record true intracycle vibratory patterns, HSDI is also considered advantageous over videostroboscopy for assessment of the normal voice. Normative HSDI studies
a
University of Tokyo Hospital, Tokyo, Japan Health Sciences University of Hokkaido, Japan c National Center for Global Health and Medicine, Tokyo, Japan b
Correspondence to Akihito Yamauchi: [email protected] Editor: Jody Kreiman Associate Editor: Scott Thomson Received August 28, 2012 Revision received December 18, 2012 Accepted June 26, 2013 DOI: 10.1044/2014_JSLHR-S-12-0269
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glottal closure, and older women demonstrated various opening and closing patterns. Both young men and older men were similar to older women. The open quotient was maximal at the most posterior glottal level in young women, but it tended to be maximal at the anterior glottis in the other subgroups. The mean value of the 5 open quotients was largest in young women. The mean speed index had a large negative value in older subjects. Conclusion: This study provides the first information about age-related differences of longitudinal oscillatory characteristics of the vocal folds obtained with high-speed digital imaging. Key Words: voice, voice disorders, endoscopy
are important for both basic vocal research and clinical application, because the data they yield are required for discrimination between normal and pathological vocal fold movements. Various authors have conducted normative HSDI studies and have reported on irregular vocal fold movements in healthy young subjects (Bonilha, Aikman, Hines, & Deliyski, 2008; Bonilha & Deliyski, 2008; Bonilha, Deliyski, & Geriach, 2008; Inwald, Döllinger, Schuster, Eysholdt, & Bohr, 2011; Kendall, 2009; Mehta, Deliyski, Quatieri, & Hillman, 2011; Shaw & Deliyski, 2008). Normative data for the geriatric population are becoming increasingly important, given the worldwide trend toward the aging of society, and they have been investigated using subjective ratings (Yamauchi et al., 2012) and laryngotopography (Yamauchi et al., 2013). So far, researchers have found that young women frequently have a posterior glottal chink and a posterior-to-anterior (PA) opening pattern, whereas young men frequently show supraglottic hyperactivity and anterior-to-posterior (AP) opening. In addition, older women often show a lateral phase difference, atrophic change, anterior glottal gap, and an AP opening pattern, whereas older men frequently demonstrate supraglottic hyperactivity, a lateral phase difference, and AP opening. Disclosure: The authors have declared that no competing interests existed at the time of publication.
Journal of Speech, Language, and Hearing Research • Vol. 57 • S648–S657 • April 2014 • A American Speech-Language-Hearing Association Supplement: Select Papers From the 8th International Conference on Vocal Physiology and Biomechanics
A high prevalence of PA opening in young women and AP opening in young men, especially during pressed phonation, has also been reported by others (Baer, Löfqvist, & McGarr, 1983; Childers, Hicks, Moore, & Alsaka, 1986; Döllinger, Lohscheller, McWhorter, & Kunduk, 2009; Hess & Ludwigs, 2000; Orlikoff, Golla, & Deliyski, 2012). Furthermore, a PA opening pattern was reported to be associated with AP closing in young women, representing zipper-like vocal fold movement (Baer et al., 1983; Childers et al., 1986; Hess & Ludwigs, 2000; Orlikoff et al., 2012). Knowledge of these normal variations of the longitudinal phase difference is important for deciding whether an HSDI film shows normal or abnormal vocal fold function. A positive correlation between the opening longitudinal phase difference and laryngeal resistance has also been reported (Yamauchi et al., 2012, 2013), but the relations among the opening longitudinal phase difference, closing longitudinal phase difference, open quotient (Oq), and speed index (SI) have not been fully described. The correlations between these parameters (the opening/ closing longitudinal phase differences, Oq, and SI) and aerodynamic or acoustic parameters have not been determined either. Accordingly, we performed HSDI in normophonic subjects together with multi-line kymography to expand our information about the time course of normophonic vocal fold movement in the longitudinal direction, to quantitatively assess age- and genderrelated differences, and to clarify the relationship of vibratory parameters with aerodynamic or acoustic variables.
Method Subjects Vocally healthy volunteers with neither vocal symptoms nor a history of laryngeal disease were recruited to participate in the present study and were divided into a young group (ages 21–35 years) and an older group (ages ≥ 65 years). All subjects were required to sign a consent form that was approved by the review board of the University of Tokyo Hospital.
Aerodynamic Studies and Acoustic Analysis We evaluated vocal function and voice quality by measuring aerodynamic and acoustic parameters. Aerodynamic parameters included the maximum phonation time (MPT), mean flow rate (MFR), and laryngeal resistance as measured by the Nagashima PE-77E Phonatory Function Analyzer (Nagashima Medical Inc., Japan). We measured acoustic variables, including the fundamental frequency (F0), amplitude perturbation quotient (APQ), period perturbation quotient (PPQ), and harmonics-to-noise ratio (Kasuya, Masubuchi, Ebihara, & Yoshida, 1986; Yumoto, Gould, & Baer, 1982), using a dedicated software program at the University of Tokyo. We chose these parameters because they are commonly investigated at Japanese voice centers.
HSDI A high-speed digital camera (FASTCAM-1024PCI; Photoron, Japan) was connected to a rigid endoscope
(No. 4450.501; Richard Wolf, USA) via an attachment lens (f = 35 mm; Nagashima Medical Inc., Japan). Recording was performed under illumination with a 300-watt xenon light source at a frame rate of 4,500 frames per second and a spatial resolution of 512 × 400 pixels, with an 8-bit gray scale and a sampling time of 1.86 s. High-speed digital images of sustained phonation of the vowel /i/ were recorded; we chose this vowel to obtain good glottal exposure while using a rigid endoscope. Phonation was performed at a conversational frequency and a comfortable vocal intensity. Acoustic and aerodynamic studies were done approximately 30 min prior to HSDI recording because simultaneous recording was not available at the University of Tokyo Hospital. However, both evaluations were done under conditions that were as similar to one another as possible to allow comparison of the parameters.
Multi-Line Kymography We performed multi-line kymography for analysis of the recorded HSDIs. All the processes for creating kymograms and measurement of parameters were done with the software program at the University of Tokyo Hospital using MATLAB. The analysis was performed as follows. First, a segment with good focus, brightness, and contrast was selected by visual inspection. Next, we set the longitudinal length to be analyzed by choosing posterior and anterior points on an HSDI image. Third, we created kymograms at five different levels so that the selected length was equally divided. Specifically, five kymograms were created at 10%, 30%, 50%, 70%, and 90% of the selected length, with 0% being set at the anterior commissure and 100% being set at the apex of the vocal process. The 10% level (the most anterior level) was labeled Position 0 and the 90% level (the most posterior level) was labeled Position 4; the intermediate levels were labeled Position 1 (the 30% level), Position 2 (the 50% level), and Position 3 (the 70% level; see Figure 1). When the landmarks (anterior commissure or vocal process) were only partially visible due to a tilted epiglottis or overhanging arytenoid, the point to be set for analysis was extrapolated from the shape of the vocal fold edge during phonation. If most of the target length was obscured, the subject was excluded from the study. Kymograms were also analyzed to determine the opening and closing longitudinal phase differences, as well as Oq and SI. At 4,500 frames per second, the frame size for analysis was 0.089 s (400 frames). Fifty-two subjects were enrolled in this study, but glottal exposure was inadequate in six subjects. Therefore, data from 46 subjects (29 women and 17 men) were analyzed, comprising 26 subjects (nine men and 17 women) in the young group and 20 subjects (eight men and 12 women) in the older group.
Opening Longitudinal Phase Difference An opening longitudinal phase difference was defined as a phase difference of glottal opening in the longitudinal direction. It was classified as PA, AP, or absent according to the pattern of glottal opening. A PA longitudinal phase
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Figure 1. A multi-line kymogram of a 21-year-old woman phonating /i/ at 269 Hz. Panel A shows a static laryngeal image at the closing phase obtained from high-speed digital imaging, and red lines signify the levels where kymograms are created. Panel B shows five obtained kymograms. Panel C shows an example of analysis: The red double arrow signifies the open phase, the yellow double arrow signifies the opening and closing phases, the yellow lines signify the starting point of the opening phase, and the blue lines signify the starting point of the closing phase. OqMLK = multi-line kymographic open quotient; SIMLK = multi-line kymographic speed index.
difference meant that opening started from the posterior glottis (Position 3 or 4) and was propagated anteriorly (Positions 0 and 1), whereas an AP difference signified that glottal opening started from the anterior glottis (Position 0 or 1) and extended posteriorly (Position 3 or 4). A longitudinal phase difference was defined as absent (“none”) if the glottal opening started at Position 2 (the mid-glottal level) and was propagated both anteriorly (to Position 1 or 0) and posteriorly (to Position 3 or 4). The magnitude of the opening longitudinal phase difference was defined as the difference between the first and last glottal opening position. Thus, it was a positive value for PA opening and a negative value for AP opening. The average magnitude of the opening longitudinal phase difference over five consecutive cycles was normalized by being divided by the glottal cycle, so the parameter was measured in degrees (range: –180° to 180°).
Closing Longitudinal Phase Difference A closing longitudinal phase difference was defined as a phase difference of glottal closure in the longitudinal direction. Similar to the opening longitudinal phase difference, the closing difference was categorized as PA, AP, or absent. The magnitude of the closing longitudinal phase difference was calculated in the same manner as that of the opening difference.
Open Quotient The Oq was calculated as the open phase divided by one glottal cycle (range: 0–1). Because multi-line kymography produces five different Oq values, the Oq of each position was
named separately; the Oq of position i (i = 0. 1, 2, 3, 4) was named as “Oqi” here (e.g., the Oq of Position 3 was Oq3). We then calculated the average of the five Oq values as the multi-line kymographic open quotient, OqMLK, which was considered to reflect overall glottal function (range: 0–1); that is, OqMLK = (Oq0 + Oq1 + Oq2 + Oq3 + Oq4)/5.
Speed Index The SI (range: –1 to 1) was calculated as follows: SI = (opening phase – closing phase)/(opening phase + closing phase). The average value of the left and right SIs for each position was named separately; the SI of position i (i = 0. 1, 2, 3, 4) was named as “SIi” here (e.g., the average SI of Position 3 was SI3), and the average of the five positional SIs was calculated as the multi-line kymographic speed index SIMLK (range: –1 to 1); that is, SIMLK = (SI0 + SI1 + SI2 + SI3 + SI4)/5.
Example of Multi-Line Kymographic Analysis Figure 1 shows the multi-line kymograms of a 21-yearold woman phonating /i/ at 269 Hz, which was the conversational frequency of this subject. Panel A shows a static laryngeal image of the closing phase obtained by HSDI, with red lines indicating the levels where kymograms were created. Panel B shows the five kymograms thus obtained, and Panel C shows an example of analysis. The red double arrow indicates the open phase. The Oq in this kymogram (Oq4) is 1.0; Oq0, Oq1, Oq2, and Oq3 are .41, .53, .65, and .82, respectively, and OqMLK is .68. The yellow double arrow indicates the opening and closing phases. In this kymogram,
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SI3 is –.21, and SI0, SI1, SI2, and SI4 are –.14, –.11, –.27, and 1.00, respectively, and SIMLK is .05. The yellow lines signify the start of the opening phase. There is a PA opening difference, and its magnitude was calculated as 127.1°. The blue lines signify the start of the closing phase. This subject has an AP closing difference, and its magnitude was calculated as –42.4°.
Demographic, Acoustic, and Aerodynamic Parameters Demographic data, aerodynamic parameters, and acoustic parameters of all subjects, along with normal values for Japanese subjects (except for the harmonics-to-noise ratio, which could not be obtained from the literature; The Japan Society of Logopedics and Phoniatrics, 2009; Nishio, Tanaka, & Niimi, 2009), are listed in Table 1. The MPT, MFR, F0, APQ, and PPQ of the participants in the present study were within the normal ranges for Japanese persons.
Statistical Analysis To investigate differences of the opening and closing longitudinal phase differences and OqMLK in relation to age or gender, we performed a one-factor analysis of variance (ANOVA). If a significant difference was identified, we then conducted a post hoc analysis (Scheffé's F test). Associations among the parameters of multi-line kymography, and associations between multi-line kymography parameters and acoustic or aerodynamic parameters, were assessed with Spearman's rank correlation analysis. Differences of p < .05 were considered significant.
Results Characteristics of Each Group Figure 2 shows the representative vocal fold vibration patterns of each group. In young women, the PA opening and AP closing pattern was predominant, representing a zipper-like action of the vocal folds (see Figure 3). The opening longitudinal phase difference was significantly larger than in the other groups (see Figure 4). For this group, Oqi and SIi increased from the anterior to posterior positions (see Figure 5) and OqMLK was large compared with the values in the other groups, whereas SIMLK was close to 0 (see Table 2). Older women frequently showed an AP opening and PA closing pattern, which was the opposite of that in young women. In older women, the absence of a closing phase difference was also frequent (see Figure 3). There was large individual variation of the magnitude of the longitudinal phase difference, which is reflected by the large standard deviation in Figure 4. We observed that Oq1 was maximal at Position 1 (the second anterior level; see Figure 5) and that SIMLK had a large negative value (see Table 2). Young men showed various patterns of the opening and closing longitudinal phase difference. For this group, Oq1 was maximal at Position 1 (see Figure 5) and SIMLK was close to 0 (see Table 2). Older men frequently showed no opening longitudinal phase difference but had various patterns of closing longitudinal phase difference. We noted that Oq1 was maximal at Position 1 (see Figure 5), OqMLK was smallest in this group, and SIMLK had a large negative value (see Table 2).
Results of ANOVA and Post Hoc Analysis Table 1. Summary of demographic data and results of aerodynamic and acoustic measures. Subgroup Women Age (years) MPT (s) MFR (ml/s) F0 (Hz) APQ (%) PPQ (%) HNR (dB) Men Age (years) MPT (s) MFR (ml/s) F0 (Hz) APQ (%) PPQ (%) HNR (dB)
Young (n = 17)
Older ( n = 12)
M ±SD 26.2 ± 3.2 23.7 ± 7.0 127.9 ± 39.2 236.3 ± 23.2 2.68 ± 1.36 0.28 ± 0.19 23.8 ± 3.9
M ±SD 71.8 ± 5.3 17.1 ± 4.8 126.5 ± 30.6 204.5 ± 45.5 3.29 ± 1.71 0.39 ± 0.60 21.7 ± 3.7
Normal value
Young (n = 9)
Older (n = 8)
29.7 ± 9.3 120.0 ± 41.0 132.0 ± 19.7 2.19 ± 0.72 0.31 ± 0.14
28.8 ± 3.1 30.5 ± 10.9 131.8 ± 41.5 119.1 ± 17.0 1.80 ± 0.91 0.16 ± 0.07 23.5 ± 4.7
74.4 ± 4.3 21.0 ± 8.5 150.6 ± 40.0 138.6 ± 24.4 3.08 ± 1.20 0.19 ± 0.11 21.2 ± 3.4
Normal value M ±SD 20.3 ± 6.7 102.0 ± 36.0 251.5 ± 24.4 2.07 ± 0.68 0.47 ± 0.32
An ANOVA, F(3, 42) = 12.9, p < .001, followed by a post hoc analysis, revealed that the opening longitudinal phase difference was significantly larger in young women than in the other groups, whereas no intergroup difference was demonstrated for the closing longitudinal phase difference, F(3, 42) = 1.42, p = .251 (see Table 2). There was a significant difference of OqMLK between young women and older men, F(3, 42) = 5.07, p = .004, and SIMLK showed a significant difference between young women and older men, as well as between young men and older men, F(3, 42) = 5.62, p = .002 (see Table 2).
Correlations
Note. Normal values are quoted from the Japanese literature (The Japan Society of Logopedics and Phoniatrics, 2009; Nishio et al., 2009). MPT = maximum phonation time; MFR = mean flow rate; APQ = amplitude perturbation quotient; PPQ = period perturbation quotient; HNR = harmonics-to-noise ratio.
The correlations between multi-line kymography parameters and selected aerodynamic or acoustic variables are given in Table 3, and the correlations among multi-line kymography parameters are shown in Table 4. The opening longitudinal phase difference demonstrated a negative correlation with the closing longitudinal phase difference (r = –.307, p < .001; see Table 4). Laryngeal resistance showed opposite correlations with the opening longitudinal phase difference (r = .280, p = .027) and the closing longitudinal phase difference (r = –.362, p = .004; see Table 3).
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Figure 2. Multi-line kymograms of representative subjects of each subgroup at conversational frequency. The red double arrow signifies the maximum open phase, the yellow lines signify the starting point of the open phase, and the blue lines signify the starting point of the closing phase.
Also, OqMLK and SIMLK were closely related to each other (r = .728, p < .001; see Table 4), and both parameters displayed a positive correlation with F0, MFR, and PPQ, as well as a negative correlation with MPT (see Table 3).
Discussion Ideally, methods of HSDI analysis should allow spatiotemporal assessment that fully describes the dynamics of vocal fold vibrations. However, current approaches are limited because the glottal area waveform method lacks information on the lateral and longitudinal directions (Yan, Chen, & Bless, 2006), whereas single-line kymography provides only mediolateral and temporal information without longitudinal information (Svec, Sram, & Schutte, 2007), and laryngotopography provides lateral and longitudinal information but lacks temporal information (Yamauchi
et al., 2013). Frame-by-frame analysis, a traditional method of assessing HSDI data by visual inspection, has the problem of subjectivity, although spatiotemporal evaluation is possible (Yamauchi et al., 2012). Phonovibrography is another suitable method for spatiotemporal assessment (Deliyski et al., 2008; Döllinger et al., 2009; Kunduk, Döllinger, McWhorter, & Lohscheller, 2010; Inwald et al., 2011). This method is especially effective for analyzing longitudinal and temporal aspects of vocal fold vibration, but mediolateral evaluation is rather complicated. Multi-line kymography is an alternative analytical method that allows objective quantitative spatiotemporal evaluation. Although longitudinal assessment is confined to five sites and is not continuous like that achieved with phonovibrography, multiline kymography has been proven to provide sufficient longitudinal information (Orlikoff et al., 2012; Tanabe, Kitajima, Gould, & Lambiase, 1975). In addition, multi-line
Figure 3. Ratios of subjects with opening/closing longitudinal phase difference are shown (ns = nine for young men, eight for older men, 17 for young women, and 12 for older men): The x-axis is a subgroup, and the y-axis is a ratio of subjects with opening/closing longitudinal phase difference.
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Figure 4. Means and standard deviations of opening/closing longitudinal phase difference of each subgroup (ns = 17 for young women, nine for young men, 12 for older women, and eight for older men): The x-axis is a horizontal level of the glottis (Position 4 is the level of vocal process, and Position 0 is the level of anterior commissure), and the y-axis is an opening/closing longitudinal phase difference described with degree (the larger the value, the earlier the glottal opening/closure).
kymography has an advantage over phonovibrography because kymographic studies are familiar to otolaryngologists, whereas phonovibrography is a novel method and interpretation of phonovibrograms requires some training. The differences between young women and men revealed in the present study support the results of previous studies. For instance, young women were also reported to show a PA opening and AP closing pattern of vocal fold movement in the previous studies performed with videostroboscopy (Biever & Bless, 1989), phonovibrography (Döllinger et al., 2009; Kunduk et al., 2010; Lohscheller, Eysholdt, Toy, & Döllinger, 2008), and multi-line kymography (Orlikoff et al., 2012). The variations of opening and closing detected in young men were also consistent with the results of other studies. Lohscheller et al. (2008) reported various patterns of glottal opening and closing in young men, although Tanabe et al. (1975) and Orlikoff et al. (2012) reported predominant AP glottal opening and PA glottal closure. The gender difference of the closing longitudinal phase difference seen in the present study (it was smaller in young men than in young women) was also reported by Orlikoff et al. (2012). Furthermore, the difference of OqMLK and similarity of SIMLK between young women and men correspond to recent data from Lohscheller, Svec, and
Döllinger (2013), who found that Oqs along the entire glottal length was .57 in males and .67 in women, while Sqs1 were .83 and .90, respectively. The present study also revealed some age-related differences, which have not been investigated by HSDI before. For instance, SIMLK was close to 0 in young subjects (the opening phase was approximately equal to the closing phase), whereas it had a large negative value in older subjects (the opening phase was shorter than the closing phase). On the other hand, OqMLK displayed both an age-related decrease and a gender-related difference (it was larger in women than men), so the influence of age was clearer for SIMLK than OqMLK. The age-related decrease of SIMLK might be explained by structural and functional alterations of the vocal folds with senescence that reduced the speed of returning to the midline. The fact that OqMLK was highest in young women might be related to a physiological posterior glottal chink that is frequently observed in this population, leading to a high Oq value at the posterior glottis (Biever & Bless, 1989; Yamauchi et al., 2012, 2013). The longitudinal
Note that Lohscheller et al. reported the “SI” value as “Sq” in their article.
1
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Figure 5. Means and standard deviations of Oqis and SIis of each subgroup (ns = 17 for young women, nine for young men, 12 for older women, and eight for older men) are shown: The x-axis is a horizontal level of the glottis (Position 4 is the level of vocal process, and Position 0 is the level of anterior commissure), and the y-axis is Oqi and SIi.
phase difference was also associated with age-related changes in women, and the opening and closing longitudinal phase differences were opposite to each other. This remarkable finding might be explained by hormonal changes. For example, estrogen is thought to cause physiological vocal fold edema by increasing capillary permeability and allowing the egress of fluid into the interstitial space, so the decline of estrogen levels in postmenopausal women would reduce vocal fold edema and lead to a decrease of vocal fold volume (Abitbol, Abitbol, & Abitbol, 1999). Anatomical and functional alterations of the larynx resulting from aging also might have a role (Kendall, 2007; Rodeno, Sanchez-Fernandez, & Rivera-Pomar, 1993). On the other hand, age-related differences were less striking in men compared to women, although lowered levels of androgen levels, which would promote vocal fold atrophy, and age-related structural and functional deterioration of the larynx, would be expected in older men (Gugatschka et al., 2010; Kendall, 2007; Rodeno et al., 1993). The relatively small number of male subjects in the present study might have led to inadequate assessment of age-related differences in men. We observed a pattern of PA opening predominantly in young women; this might be explained by a combination of strong anterior glottal closure and weak posterior glottal closure, so that the posterior glottis opens more readily than the
anterior glottis (Hess & Ludwigs, 2000). Physiological vocal fold edema in young female subjects resulting from high estrogen and progesterone levels might lead to elevated glottal resistance and strengthen anterior glottal closure (Abitbol et al., 1999; Biever & Bless, 1989; Gugatschka et al., 2010). The cricothyroid and posterior cricothyroid muscles might also have an influence. These two muscles are active during high frequency phonation, tensing and slightly abducting the vocal folds to produce a posterior glottal chink or weak closure of the posterior glottis (The Japan Society of Logopedics and Phoniatrics, 2009). The positive correlation between F0 and the opening longitudinal phase difference revealed in the present study might be explained by activation of the cricothyroid and posterior cricothyroid muscles during phonation with high F0, versus predominant activation of the thyroarytenoid muscles during phonation with low F0 (The Japan Society of Logopedics and Phoniatrics, 2009). Likewise, an AP opening pattern might be explained by weak anterior glottal closure and strong posterior glottal closure. This could occur, for example, when there is atrophy of the laryngeal musculature and submucosal tissue, weakened adduction of the intrinsic laryngeal muscles resulting from geriatric changes (Kendall, 2007; Rodeno et al., 1993), or reduced decrease of vocal fold edema resulting from lower estrogen levels, which has been reported in both older men and
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Table 2. Results of a post hoc analysis (M±SD) among subgroups regarding parameters of multi-line kymography.
Parameter
ANOVA (p)
YW
YM
OW
OM
Opening LPD
107.0 ± 60.0
–9.1 ± 55.2
–26.5 ± 91.2
–21.5 ± 45.3
< .01
Closing LPD OqMLK
–18.9 ± 17.8 0.61 ± 0.10
–2.9 ± 30.8 0.47 ± 0.13
–4.6 ± 76.9 0.53 ± 0.13
25.3 ± 62.8 0.40 ± 0.07
.25 < .01
–0.05 ± 0.12
–0.04 ± 0.24
–0.22 ± 0.18
–0.28 ± 0.14
< .01
MLK
SI
Post hoc analysis (pair with significant difference) YW and YM** YW and OW** YW and OM** YW and YM* YW and OM* YW and OM* YM and OM*
Note. YW = young women; YM = young men; OW = older women; OM = older men; ANOVA = analysis of variance; LPD = longitudinal phase difference. *p < .05. **p < .01.
older women (Abitbol et al., 1999; Gugatschka et al., 2010). The association between an AP opening pattern and low laryngeal resistance seems to support such speculation. However, some authors have reported an association between AP opening and pressed phonation (Granqvist, Hertegård, Larsson, & Sundberg, 2003; Hess et al., 2000): Hess et al. (2000) speculated that strong contact stress predominantly affects the cartilaginous portion of the vocal folds, leading to air escape at the point of least resistance, which is assumed to be the anterior membranous portion. Further investigation of the AP opening longitudinal phase difference is required because various mechanisms may be involved. According to the literature, the closing phase is mainly influenced by intrinsic vocal fold material properties that determine the speed of vocal fold return to the midline, whereas the opening phase is influenced by several factors, such as vocal fold geometry, subglottal pressure, and vocal fold material properties (Titze, 1988). The results obtained in the present study support this concept because the closing longitudinal phase difference was a mirror image of the opening longitudinal phase difference (e.g., the predominance of AP closure in young women and the negative correlation with laryngeal resistance). The closing longitudinal phase difference could more sensitively reflect alterations of vocal fold material properties or function than the opening longitudinal phase difference in some circumstances. Döllinger et al. (2009) reported a decrease of the closing longitudinal phase difference after performance of a vocal Table 3. Correlations between parameters of multi-line kymography.
Parameter MPT MFR Laryngeal resistance HNR APQ PPQ F0
Opening LPD
Closing LPD
OqMLK
SIMLK
.086 –.182 .280* .217 .064 –.020 .336**
.028 .073 –.362** –.188 .088 .036 –.130
–.457*** .485*** .058 –.137 .075 .417*** .232
–.399** .460*** .031 –.038 –.021 .288* .382**
*p < .05. **p < .01. ***p < .001.
loading task in a female subject, although there was no significant change of the opening longitudinal phase difference. In the present study, there was an age-related difference with respect to the standard deviation of the closing longitudinal phase difference, but not the opening longitudinal phase difference. The present study not only adds to the normative HSDI database, which is relatively small, but also demonstrates gender- and age-related differences among healthy subjects, which have never been investigated by HSDI before. The present results should encourage further clinical application of multi-line kymography. For instance, the longitudinal phase difference might be used in the clinical setting to assess laryngeal resistance, with detection of an AP opening pattern in a young woman, prompting the clinician to search for pathology associated with weak laryngeal resistance such as vocal fold atrophy. Because OqMLK and SIMLK were significantly correlated with aerodynamic parameters (e.g., MPT and MFR) as well as acoustic parameters (e.g., F0 and PPQ), they might also be applied clinically as indicators of the severity of dysphonia. The present study had several limitations. First, detailed changes related to age could not be described because of the lack of middle-age and adolescent subjects. Second, the analysis method was not automated and was time consuming. Third, simultaneous recording of HSDI and aerodynamic or acoustic parameters was not available, which presumably led to relatively low correlations. In the future, studies need to be conducted with different samples, especially the middle-aged population. In addition, an automated analysis system should be developed, as should methods Table 4. Correlations among parameters of multi-line kymography. Variable
1
2
3
4
1. 2. 3. 4.
—
–.307*** —
.398*** –.162* —
.225*** –.045 .728*** —
Opening LPD Closing LPD Oqi SIi
*p < .05. ***p < .001.
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for simultaneous recording of HSDI and aerodynamic or acoustic parameters. Furthermore, HSDI studies should be performed with samples of individuals with various laryngeal diseases.
Conclusion The present study provides the first information about age-related differences of longitudinal oscillatory characteristics of the vocal folds using HSDI. Young women frequently displayed longitudinal phase differences such as PA opening and AP closing, resulting in zipper-like vocal fold movements. The vibratory patterns seen in young women were quite different from those seen in older women, who displayed various longitudinal phase differences of opening and closing, which resembled the findings in young men and older men. Age-related differences of OqMLK and SIMLK were also observed. Clinicians should be aware of these findings so they will be able to distinguish normality from abnormality and avoid overdiagnosis. Opening and closing longitudinal phase differences, as well as OqMLK and SIMLK, might be used clinically to assess laryngeal resistance and the severity of dysphonia, respectively.
Acknowledgments This research was presented at the 8th International Conference on Voice Physiology and Biomechanics, Erlangen, Germany, 2012.
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Svec, J. G., Sram, F., & Schutte, H. K. (2007). Videokymography in voice disorders: What to look for? Annals of Otology, Rhinology & Laryngology, 116, 172–180. Tanabe, M., Kitajima, K., Gould, W. J., & Lambiase, A. (1975). Analysis of high-speed motion pictures of the vocal folds. Folia Phoniatrica et Logopaedica, 27, 77–87. Titze, I. R. (1988). The physics of small-amplitude oscillation of the vocal folds. The Journal of the Acoustical Society of America, 83, 1536–1552. Verikas, A., Uloza, V., Bacauskiene, M., Gelzinis, A., & Kelertas, E. (2009). Advances in laryngeal imaging. European Archives of Oto-Rhino-Laryngology, 266, 1509–1520. Yamauchi, A., Imagawa, H., Sakakibara, K-I., Yokonishi, H., Nito, T., Yamasoba, T., & Tayama, N. (2013). Phase difference
of vocally healthy subjects in high-speed digital imaging analyzed with laryngotopography. Journal of Voice, 27, 39–45. Yamauchi, A., Imagawa, H., Yokonishi, H., Nito, T., Yamasoba, T., Goto, T., . . . Tayama, N. (2012). Evaluation of vocal fold vibration with an assessment form for high-speed digital imaging: Comparative study between healthy young and elderly subjects. Journal of Voice, 26, 742–750. Yan, Y., Chen, X., & Bless, D. (2006). Automatic tracing of vocalfold motion from high-speed digital images. IEEE Transactions on Biomedical Engineering, 53, 1394–1400. Yumoto, E., Gould, W. J., & Baer, T. (1982). Harmonics-to-noise ratio as an index of the degree of hoarseness. The Journal of the Acoustical Society of America, 71, 1544–1550.
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Characteristics of Vocal Fold Vibrations in Vocally Healthy Subjects: Analysis With Multi-Line Kymography Akihito Yamauchi,a Hiroshi Imagawa,a Ken-Ichi Sakakibara,b Hisayuki Yokonishi,a Takaharu Nito,a Tatsuya Yamasoba,a and Niro Tayamac
Purpose: In this study, the authors aimed to analyze longitudinal data from high-speed digital images in normative subjects using multi-line kymography. Method: Vocally healthy subjects were divided into young (9 men and 17 women; Mage = 27 years) and older groups (8 men and 12 women; Mage = 73 years). From high-speed digital images of phonation at a conversational frequency kymograms were created at 5 different levels of the vocal fold and were analyzed to determine the opening/closing longitudinal phase difference, open quotient, and speed index. Then age- and gender-related differences of these parameters were analyzed statistically. Results: Young women frequently showed a pattern of posterior-to-anterior glottal opening and anterior-to-posterior
V
ideostroboscopy is widely used for the observation of vocal fold vibrations (Deliyski & Hillman, 2010; Verikas, Uloza, Bacauskiene, Gelzinis, & Kelertas, 2009). However, preceding periodic phonation with a stable fundamental frequency is needed for the production of videostroboscopic oscillating images, which means that videostroboscopy is not applicable to unstable phonation, such as transient, subharmonic, or aperiodic phonation. For the observation of such unstable vocal fold dynamics, highspeed digital imaging (HSDI) is considered more suitable (Kendall, 2009; Olthoff, Woywod, & Kruse, 2007; Patel, Dailey, & Bless, 2008). Because it can record true intracycle vibratory patterns, HSDI is also considered advantageous over videostroboscopy for assessment of the normal voice. Normative HSDI studies
a
University of Tokyo Hospital, Tokyo, Japan Health Sciences University of Hokkaido, Japan c National Center for Global Health and Medicine, Tokyo, Japan b
Correspondence to Akihito Yamauchi: [email protected] Editor: Jody Kreiman Associate Editor: Scott Thomson Received August 28, 2012 Revision received December 18, 2012 Accepted June 26, 2013 DOI: 10.1044/2014_JSLHR-S-12-0269
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glottal closure, and older women demonstrated various opening and closing patterns. Both young men and older men were similar to older women. The open quotient was maximal at the most posterior glottal level in young women, but it tended to be maximal at the anterior glottis in the other subgroups. The mean value of the 5 open quotients was largest in young women. The mean speed index had a large negative value in older subjects. Conclusion: This study provides the first information about age-related differences of longitudinal oscillatory characteristics of the vocal folds obtained with high-speed digital imaging. Key Words: voice, voice disorders, endoscopy
are important for both basic vocal research and clinical application, because the data they yield are required for discrimination between normal and pathological vocal fold movements. Various authors have conducted normative HSDI studies and have reported on irregular vocal fold movements in healthy young subjects (Bonilha, Aikman, Hines, & Deliyski, 2008; Bonilha & Deliyski, 2008; Bonilha, Deliyski, & Geriach, 2008; Inwald, Döllinger, Schuster, Eysholdt, & Bohr, 2011; Kendall, 2009; Mehta, Deliyski, Quatieri, & Hillman, 2011; Shaw & Deliyski, 2008). Normative data for the geriatric population are becoming increasingly important, given the worldwide trend toward the aging of society, and they have been investigated using subjective ratings (Yamauchi et al., 2012) and laryngotopography (Yamauchi et al., 2013). So far, researchers have found that young women frequently have a posterior glottal chink and a posterior-to-anterior (PA) opening pattern, whereas young men frequently show supraglottic hyperactivity and anterior-to-posterior (AP) opening. In addition, older women often show a lateral phase difference, atrophic change, anterior glottal gap, and an AP opening pattern, whereas older men frequently demonstrate supraglottic hyperactivity, a lateral phase difference, and AP opening. Disclosure: The authors have declared that no competing interests existed at the time of publication.
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A high prevalence of PA opening in young women and AP opening in young men, especially during pressed phonation, has also been reported by others (Baer, Löfqvist, & McGarr, 1983; Childers, Hicks, Moore, & Alsaka, 1986; Döllinger, Lohscheller, McWhorter, & Kunduk, 2009; Hess & Ludwigs, 2000; Orlikoff, Golla, & Deliyski, 2012). Furthermore, a PA opening pattern was reported to be associated with AP closing in young women, representing zipper-like vocal fold movement (Baer et al., 1983; Childers et al., 1986; Hess & Ludwigs, 2000; Orlikoff et al., 2012). Knowledge of these normal variations of the longitudinal phase difference is important for deciding whether an HSDI film shows normal or abnormal vocal fold function. A positive correlation between the opening longitudinal phase difference and laryngeal resistance has also been reported (Yamauchi et al., 2012, 2013), but the relations among the opening longitudinal phase difference, closing longitudinal phase difference, open quotient (Oq), and speed index (SI) have not been fully described. The correlations between these parameters (the opening/ closing longitudinal phase differences, Oq, and SI) and aerodynamic or acoustic parameters have not been determined either. Accordingly, we performed HSDI in normophonic subjects together with multi-line kymography to expand our information about the time course of normophonic vocal fold movement in the longitudinal direction, to quantitatively assess age- and genderrelated differences, and to clarify the relationship of vibratory parameters with aerodynamic or acoustic variables.
Method Subjects Vocally healthy volunteers with neither vocal symptoms nor a history of laryngeal disease were recruited to participate in the present study and were divided into a young group (ages 21–35 years) and an older group (ages ≥ 65 years). All subjects were required to sign a consent form that was approved by the review board of the University of Tokyo Hospital.
Aerodynamic Studies and Acoustic Analysis We evaluated vocal function and voice quality by measuring aerodynamic and acoustic parameters. Aerodynamic parameters included the maximum phonation time (MPT), mean flow rate (MFR), and laryngeal resistance as measured by the Nagashima PE-77E Phonatory Function Analyzer (Nagashima Medical Inc., Japan). We measured acoustic variables, including the fundamental frequency (F0), amplitude perturbation quotient (APQ), period perturbation quotient (PPQ), and harmonics-to-noise ratio (Kasuya, Masubuchi, Ebihara, & Yoshida, 1986; Yumoto, Gould, & Baer, 1982), using a dedicated software program at the University of Tokyo. We chose these parameters because they are commonly investigated at Japanese voice centers.
HSDI A high-speed digital camera (FASTCAM-1024PCI; Photoron, Japan) was connected to a rigid endoscope
(No. 4450.501; Richard Wolf, USA) via an attachment lens (f = 35 mm; Nagashima Medical Inc., Japan). Recording was performed under illumination with a 300-watt xenon light source at a frame rate of 4,500 frames per second and a spatial resolution of 512 × 400 pixels, with an 8-bit gray scale and a sampling time of 1.86 s. High-speed digital images of sustained phonation of the vowel /i/ were recorded; we chose this vowel to obtain good glottal exposure while using a rigid endoscope. Phonation was performed at a conversational frequency and a comfortable vocal intensity. Acoustic and aerodynamic studies were done approximately 30 min prior to HSDI recording because simultaneous recording was not available at the University of Tokyo Hospital. However, both evaluations were done under conditions that were as similar to one another as possible to allow comparison of the parameters.
Multi-Line Kymography We performed multi-line kymography for analysis of the recorded HSDIs. All the processes for creating kymograms and measurement of parameters were done with the software program at the University of Tokyo Hospital using MATLAB. The analysis was performed as follows. First, a segment with good focus, brightness, and contrast was selected by visual inspection. Next, we set the longitudinal length to be analyzed by choosing posterior and anterior points on an HSDI image. Third, we created kymograms at five different levels so that the selected length was equally divided. Specifically, five kymograms were created at 10%, 30%, 50%, 70%, and 90% of the selected length, with 0% being set at the anterior commissure and 100% being set at the apex of the vocal process. The 10% level (the most anterior level) was labeled Position 0 and the 90% level (the most posterior level) was labeled Position 4; the intermediate levels were labeled Position 1 (the 30% level), Position 2 (the 50% level), and Position 3 (the 70% level; see Figure 1). When the landmarks (anterior commissure or vocal process) were only partially visible due to a tilted epiglottis or overhanging arytenoid, the point to be set for analysis was extrapolated from the shape of the vocal fold edge during phonation. If most of the target length was obscured, the subject was excluded from the study. Kymograms were also analyzed to determine the opening and closing longitudinal phase differences, as well as Oq and SI. At 4,500 frames per second, the frame size for analysis was 0.089 s (400 frames). Fifty-two subjects were enrolled in this study, but glottal exposure was inadequate in six subjects. Therefore, data from 46 subjects (29 women and 17 men) were analyzed, comprising 26 subjects (nine men and 17 women) in the young group and 20 subjects (eight men and 12 women) in the older group.
Opening Longitudinal Phase Difference An opening longitudinal phase difference was defined as a phase difference of glottal opening in the longitudinal direction. It was classified as PA, AP, or absent according to the pattern of glottal opening. A PA longitudinal phase
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Figure 1. A multi-line kymogram of a 21-year-old woman phonating /i/ at 269 Hz. Panel A shows a static laryngeal image at the closing phase obtained from high-speed digital imaging, and red lines signify the levels where kymograms are created. Panel B shows five obtained kymograms. Panel C shows an example of analysis: The red double arrow signifies the open phase, the yellow double arrow signifies the opening and closing phases, the yellow lines signify the starting point of the opening phase, and the blue lines signify the starting point of the closing phase. OqMLK = multi-line kymographic open quotient; SIMLK = multi-line kymographic speed index.
difference meant that opening started from the posterior glottis (Position 3 or 4) and was propagated anteriorly (Positions 0 and 1), whereas an AP difference signified that glottal opening started from the anterior glottis (Position 0 or 1) and extended posteriorly (Position 3 or 4). A longitudinal phase difference was defined as absent (“none”) if the glottal opening started at Position 2 (the mid-glottal level) and was propagated both anteriorly (to Position 1 or 0) and posteriorly (to Position 3 or 4). The magnitude of the opening longitudinal phase difference was defined as the difference between the first and last glottal opening position. Thus, it was a positive value for PA opening and a negative value for AP opening. The average magnitude of the opening longitudinal phase difference over five consecutive cycles was normalized by being divided by the glottal cycle, so the parameter was measured in degrees (range: –180° to 180°).
Closing Longitudinal Phase Difference A closing longitudinal phase difference was defined as a phase difference of glottal closure in the longitudinal direction. Similar to the opening longitudinal phase difference, the closing difference was categorized as PA, AP, or absent. The magnitude of the closing longitudinal phase difference was calculated in the same manner as that of the opening difference.
Open Quotient The Oq was calculated as the open phase divided by one glottal cycle (range: 0–1). Because multi-line kymography produces five different Oq values, the Oq of each position was
named separately; the Oq of position i (i = 0. 1, 2, 3, 4) was named as “Oqi” here (e.g., the Oq of Position 3 was Oq3). We then calculated the average of the five Oq values as the multi-line kymographic open quotient, OqMLK, which was considered to reflect overall glottal function (range: 0–1); that is, OqMLK = (Oq0 + Oq1 + Oq2 + Oq3 + Oq4)/5.
Speed Index The SI (range: –1 to 1) was calculated as follows: SI = (opening phase – closing phase)/(opening phase + closing phase). The average value of the left and right SIs for each position was named separately; the SI of position i (i = 0. 1, 2, 3, 4) was named as “SIi” here (e.g., the average SI of Position 3 was SI3), and the average of the five positional SIs was calculated as the multi-line kymographic speed index SIMLK (range: –1 to 1); that is, SIMLK = (SI0 + SI1 + SI2 + SI3 + SI4)/5.
Example of Multi-Line Kymographic Analysis Figure 1 shows the multi-line kymograms of a 21-yearold woman phonating /i/ at 269 Hz, which was the conversational frequency of this subject. Panel A shows a static laryngeal image of the closing phase obtained by HSDI, with red lines indicating the levels where kymograms were created. Panel B shows the five kymograms thus obtained, and Panel C shows an example of analysis. The red double arrow indicates the open phase. The Oq in this kymogram (Oq4) is 1.0; Oq0, Oq1, Oq2, and Oq3 are .41, .53, .65, and .82, respectively, and OqMLK is .68. The yellow double arrow indicates the opening and closing phases. In this kymogram,
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SI3 is –.21, and SI0, SI1, SI2, and SI4 are –.14, –.11, –.27, and 1.00, respectively, and SIMLK is .05. The yellow lines signify the start of the opening phase. There is a PA opening difference, and its magnitude was calculated as 127.1°. The blue lines signify the start of the closing phase. This subject has an AP closing difference, and its magnitude was calculated as –42.4°.
Demographic, Acoustic, and Aerodynamic Parameters Demographic data, aerodynamic parameters, and acoustic parameters of all subjects, along with normal values for Japanese subjects (except for the harmonics-to-noise ratio, which could not be obtained from the literature; The Japan Society of Logopedics and Phoniatrics, 2009; Nishio, Tanaka, & Niimi, 2009), are listed in Table 1. The MPT, MFR, F0, APQ, and PPQ of the participants in the present study were within the normal ranges for Japanese persons.
Statistical Analysis To investigate differences of the opening and closing longitudinal phase differences and OqMLK in relation to age or gender, we performed a one-factor analysis of variance (ANOVA). If a significant difference was identified, we then conducted a post hoc analysis (Scheffé's F test). Associations among the parameters of multi-line kymography, and associations between multi-line kymography parameters and acoustic or aerodynamic parameters, were assessed with Spearman's rank correlation analysis. Differences of p < .05 were considered significant.
Results Characteristics of Each Group Figure 2 shows the representative vocal fold vibration patterns of each group. In young women, the PA opening and AP closing pattern was predominant, representing a zipper-like action of the vocal folds (see Figure 3). The opening longitudinal phase difference was significantly larger than in the other groups (see Figure 4). For this group, Oqi and SIi increased from the anterior to posterior positions (see Figure 5) and OqMLK was large compared with the values in the other groups, whereas SIMLK was close to 0 (see Table 2). Older women frequently showed an AP opening and PA closing pattern, which was the opposite of that in young women. In older women, the absence of a closing phase difference was also frequent (see Figure 3). There was large individual variation of the magnitude of the longitudinal phase difference, which is reflected by the large standard deviation in Figure 4. We observed that Oq1 was maximal at Position 1 (the second anterior level; see Figure 5) and that SIMLK had a large negative value (see Table 2). Young men showed various patterns of the opening and closing longitudinal phase difference. For this group, Oq1 was maximal at Position 1 (see Figure 5) and SIMLK was close to 0 (see Table 2). Older men frequently showed no opening longitudinal phase difference but had various patterns of closing longitudinal phase difference. We noted that Oq1 was maximal at Position 1 (see Figure 5), OqMLK was smallest in this group, and SIMLK had a large negative value (see Table 2).
Results of ANOVA and Post Hoc Analysis Table 1. Summary of demographic data and results of aerodynamic and acoustic measures. Subgroup Women Age (years) MPT (s) MFR (ml/s) F0 (Hz) APQ (%) PPQ (%) HNR (dB) Men Age (years) MPT (s) MFR (ml/s) F0 (Hz) APQ (%) PPQ (%) HNR (dB)
Young (n = 17)
Older ( n = 12)
M ±SD 26.2 ± 3.2 23.7 ± 7.0 127.9 ± 39.2 236.3 ± 23.2 2.68 ± 1.36 0.28 ± 0.19 23.8 ± 3.9
M ±SD 71.8 ± 5.3 17.1 ± 4.8 126.5 ± 30.6 204.5 ± 45.5 3.29 ± 1.71 0.39 ± 0.60 21.7 ± 3.7
Normal value
Young (n = 9)
Older (n = 8)
29.7 ± 9.3 120.0 ± 41.0 132.0 ± 19.7 2.19 ± 0.72 0.31 ± 0.14
28.8 ± 3.1 30.5 ± 10.9 131.8 ± 41.5 119.1 ± 17.0 1.80 ± 0.91 0.16 ± 0.07 23.5 ± 4.7
74.4 ± 4.3 21.0 ± 8.5 150.6 ± 40.0 138.6 ± 24.4 3.08 ± 1.20 0.19 ± 0.11 21.2 ± 3.4
Normal value M ±SD 20.3 ± 6.7 102.0 ± 36.0 251.5 ± 24.4 2.07 ± 0.68 0.47 ± 0.32
An ANOVA, F(3, 42) = 12.9, p < .001, followed by a post hoc analysis, revealed that the opening longitudinal phase difference was significantly larger in young women than in the other groups, whereas no intergroup difference was demonstrated for the closing longitudinal phase difference, F(3, 42) = 1.42, p = .251 (see Table 2). There was a significant difference of OqMLK between young women and older men, F(3, 42) = 5.07, p = .004, and SIMLK showed a significant difference between young women and older men, as well as between young men and older men, F(3, 42) = 5.62, p = .002 (see Table 2).
Correlations
Note. Normal values are quoted from the Japanese literature (The Japan Society of Logopedics and Phoniatrics, 2009; Nishio et al., 2009). MPT = maximum phonation time; MFR = mean flow rate; APQ = amplitude perturbation quotient; PPQ = period perturbation quotient; HNR = harmonics-to-noise ratio.
The correlations between multi-line kymography parameters and selected aerodynamic or acoustic variables are given in Table 3, and the correlations among multi-line kymography parameters are shown in Table 4. The opening longitudinal phase difference demonstrated a negative correlation with the closing longitudinal phase difference (r = –.307, p < .001; see Table 4). Laryngeal resistance showed opposite correlations with the opening longitudinal phase difference (r = .280, p = .027) and the closing longitudinal phase difference (r = –.362, p = .004; see Table 3).
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Figure 2. Multi-line kymograms of representative subjects of each subgroup at conversational frequency. The red double arrow signifies the maximum open phase, the yellow lines signify the starting point of the open phase, and the blue lines signify the starting point of the closing phase.
Also, OqMLK and SIMLK were closely related to each other (r = .728, p < .001; see Table 4), and both parameters displayed a positive correlation with F0, MFR, and PPQ, as well as a negative correlation with MPT (see Table 3).
Discussion Ideally, methods of HSDI analysis should allow spatiotemporal assessment that fully describes the dynamics of vocal fold vibrations. However, current approaches are limited because the glottal area waveform method lacks information on the lateral and longitudinal directions (Yan, Chen, & Bless, 2006), whereas single-line kymography provides only mediolateral and temporal information without longitudinal information (Svec, Sram, & Schutte, 2007), and laryngotopography provides lateral and longitudinal information but lacks temporal information (Yamauchi
et al., 2013). Frame-by-frame analysis, a traditional method of assessing HSDI data by visual inspection, has the problem of subjectivity, although spatiotemporal evaluation is possible (Yamauchi et al., 2012). Phonovibrography is another suitable method for spatiotemporal assessment (Deliyski et al., 2008; Döllinger et al., 2009; Kunduk, Döllinger, McWhorter, & Lohscheller, 2010; Inwald et al., 2011). This method is especially effective for analyzing longitudinal and temporal aspects of vocal fold vibration, but mediolateral evaluation is rather complicated. Multi-line kymography is an alternative analytical method that allows objective quantitative spatiotemporal evaluation. Although longitudinal assessment is confined to five sites and is not continuous like that achieved with phonovibrography, multiline kymography has been proven to provide sufficient longitudinal information (Orlikoff et al., 2012; Tanabe, Kitajima, Gould, & Lambiase, 1975). In addition, multi-line
Figure 3. Ratios of subjects with opening/closing longitudinal phase difference are shown (ns = nine for young men, eight for older men, 17 for young women, and 12 for older men): The x-axis is a subgroup, and the y-axis is a ratio of subjects with opening/closing longitudinal phase difference.
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Figure 4. Means and standard deviations of opening/closing longitudinal phase difference of each subgroup (ns = 17 for young women, nine for young men, 12 for older women, and eight for older men): The x-axis is a horizontal level of the glottis (Position 4 is the level of vocal process, and Position 0 is the level of anterior commissure), and the y-axis is an opening/closing longitudinal phase difference described with degree (the larger the value, the earlier the glottal opening/closure).
kymography has an advantage over phonovibrography because kymographic studies are familiar to otolaryngologists, whereas phonovibrography is a novel method and interpretation of phonovibrograms requires some training. The differences between young women and men revealed in the present study support the results of previous studies. For instance, young women were also reported to show a PA opening and AP closing pattern of vocal fold movement in the previous studies performed with videostroboscopy (Biever & Bless, 1989), phonovibrography (Döllinger et al., 2009; Kunduk et al., 2010; Lohscheller, Eysholdt, Toy, & Döllinger, 2008), and multi-line kymography (Orlikoff et al., 2012). The variations of opening and closing detected in young men were also consistent with the results of other studies. Lohscheller et al. (2008) reported various patterns of glottal opening and closing in young men, although Tanabe et al. (1975) and Orlikoff et al. (2012) reported predominant AP glottal opening and PA glottal closure. The gender difference of the closing longitudinal phase difference seen in the present study (it was smaller in young men than in young women) was also reported by Orlikoff et al. (2012). Furthermore, the difference of OqMLK and similarity of SIMLK between young women and men correspond to recent data from Lohscheller, Svec, and
Döllinger (2013), who found that Oqs along the entire glottal length was .57 in males and .67 in women, while Sqs1 were .83 and .90, respectively. The present study also revealed some age-related differences, which have not been investigated by HSDI before. For instance, SIMLK was close to 0 in young subjects (the opening phase was approximately equal to the closing phase), whereas it had a large negative value in older subjects (the opening phase was shorter than the closing phase). On the other hand, OqMLK displayed both an age-related decrease and a gender-related difference (it was larger in women than men), so the influence of age was clearer for SIMLK than OqMLK. The age-related decrease of SIMLK might be explained by structural and functional alterations of the vocal folds with senescence that reduced the speed of returning to the midline. The fact that OqMLK was highest in young women might be related to a physiological posterior glottal chink that is frequently observed in this population, leading to a high Oq value at the posterior glottis (Biever & Bless, 1989; Yamauchi et al., 2012, 2013). The longitudinal
Note that Lohscheller et al. reported the “SI” value as “Sq” in their article.
1
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Figure 5. Means and standard deviations of Oqis and SIis of each subgroup (ns = 17 for young women, nine for young men, 12 for older women, and eight for older men) are shown: The x-axis is a horizontal level of the glottis (Position 4 is the level of vocal process, and Position 0 is the level of anterior commissure), and the y-axis is Oqi and SIi.
phase difference was also associated with age-related changes in women, and the opening and closing longitudinal phase differences were opposite to each other. This remarkable finding might be explained by hormonal changes. For example, estrogen is thought to cause physiological vocal fold edema by increasing capillary permeability and allowing the egress of fluid into the interstitial space, so the decline of estrogen levels in postmenopausal women would reduce vocal fold edema and lead to a decrease of vocal fold volume (Abitbol, Abitbol, & Abitbol, 1999). Anatomical and functional alterations of the larynx resulting from aging also might have a role (Kendall, 2007; Rodeno, Sanchez-Fernandez, & Rivera-Pomar, 1993). On the other hand, age-related differences were less striking in men compared to women, although lowered levels of androgen levels, which would promote vocal fold atrophy, and age-related structural and functional deterioration of the larynx, would be expected in older men (Gugatschka et al., 2010; Kendall, 2007; Rodeno et al., 1993). The relatively small number of male subjects in the present study might have led to inadequate assessment of age-related differences in men. We observed a pattern of PA opening predominantly in young women; this might be explained by a combination of strong anterior glottal closure and weak posterior glottal closure, so that the posterior glottis opens more readily than the
anterior glottis (Hess & Ludwigs, 2000). Physiological vocal fold edema in young female subjects resulting from high estrogen and progesterone levels might lead to elevated glottal resistance and strengthen anterior glottal closure (Abitbol et al., 1999; Biever & Bless, 1989; Gugatschka et al., 2010). The cricothyroid and posterior cricothyroid muscles might also have an influence. These two muscles are active during high frequency phonation, tensing and slightly abducting the vocal folds to produce a posterior glottal chink or weak closure of the posterior glottis (The Japan Society of Logopedics and Phoniatrics, 2009). The positive correlation between F0 and the opening longitudinal phase difference revealed in the present study might be explained by activation of the cricothyroid and posterior cricothyroid muscles during phonation with high F0, versus predominant activation of the thyroarytenoid muscles during phonation with low F0 (The Japan Society of Logopedics and Phoniatrics, 2009). Likewise, an AP opening pattern might be explained by weak anterior glottal closure and strong posterior glottal closure. This could occur, for example, when there is atrophy of the laryngeal musculature and submucosal tissue, weakened adduction of the intrinsic laryngeal muscles resulting from geriatric changes (Kendall, 2007; Rodeno et al., 1993), or reduced decrease of vocal fold edema resulting from lower estrogen levels, which has been reported in both older men and
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Table 2. Results of a post hoc analysis (M±SD) among subgroups regarding parameters of multi-line kymography.
Parameter
ANOVA (p)
YW
YM
OW
OM
Opening LPD
107.0 ± 60.0
–9.1 ± 55.2
–26.5 ± 91.2
–21.5 ± 45.3
< .01
Closing LPD OqMLK
–18.9 ± 17.8 0.61 ± 0.10
–2.9 ± 30.8 0.47 ± 0.13
–4.6 ± 76.9 0.53 ± 0.13
25.3 ± 62.8 0.40 ± 0.07
.25 < .01
–0.05 ± 0.12
–0.04 ± 0.24
–0.22 ± 0.18
–0.28 ± 0.14
< .01
MLK
SI
Post hoc analysis (pair with significant difference) YW and YM** YW and OW** YW and OM** YW and YM* YW and OM* YW and OM* YM and OM*
Note. YW = young women; YM = young men; OW = older women; OM = older men; ANOVA = analysis of variance; LPD = longitudinal phase difference. *p < .05. **p < .01.
older women (Abitbol et al., 1999; Gugatschka et al., 2010). The association between an AP opening pattern and low laryngeal resistance seems to support such speculation. However, some authors have reported an association between AP opening and pressed phonation (Granqvist, Hertegård, Larsson, & Sundberg, 2003; Hess et al., 2000): Hess et al. (2000) speculated that strong contact stress predominantly affects the cartilaginous portion of the vocal folds, leading to air escape at the point of least resistance, which is assumed to be the anterior membranous portion. Further investigation of the AP opening longitudinal phase difference is required because various mechanisms may be involved. According to the literature, the closing phase is mainly influenced by intrinsic vocal fold material properties that determine the speed of vocal fold return to the midline, whereas the opening phase is influenced by several factors, such as vocal fold geometry, subglottal pressure, and vocal fold material properties (Titze, 1988). The results obtained in the present study support this concept because the closing longitudinal phase difference was a mirror image of the opening longitudinal phase difference (e.g., the predominance of AP closure in young women and the negative correlation with laryngeal resistance). The closing longitudinal phase difference could more sensitively reflect alterations of vocal fold material properties or function than the opening longitudinal phase difference in some circumstances. Döllinger et al. (2009) reported a decrease of the closing longitudinal phase difference after performance of a vocal Table 3. Correlations between parameters of multi-line kymography.
Parameter MPT MFR Laryngeal resistance HNR APQ PPQ F0
Opening LPD
Closing LPD
OqMLK
SIMLK
.086 –.182 .280* .217 .064 –.020 .336**
.028 .073 –.362** –.188 .088 .036 –.130
–.457*** .485*** .058 –.137 .075 .417*** .232
–.399** .460*** .031 –.038 –.021 .288* .382**
*p < .05. **p < .01. ***p < .001.
loading task in a female subject, although there was no significant change of the opening longitudinal phase difference. In the present study, there was an age-related difference with respect to the standard deviation of the closing longitudinal phase difference, but not the opening longitudinal phase difference. The present study not only adds to the normative HSDI database, which is relatively small, but also demonstrates gender- and age-related differences among healthy subjects, which have never been investigated by HSDI before. The present results should encourage further clinical application of multi-line kymography. For instance, the longitudinal phase difference might be used in the clinical setting to assess laryngeal resistance, with detection of an AP opening pattern in a young woman, prompting the clinician to search for pathology associated with weak laryngeal resistance such as vocal fold atrophy. Because OqMLK and SIMLK were significantly correlated with aerodynamic parameters (e.g., MPT and MFR) as well as acoustic parameters (e.g., F0 and PPQ), they might also be applied clinically as indicators of the severity of dysphonia. The present study had several limitations. First, detailed changes related to age could not be described because of the lack of middle-age and adolescent subjects. Second, the analysis method was not automated and was time consuming. Third, simultaneous recording of HSDI and aerodynamic or acoustic parameters was not available, which presumably led to relatively low correlations. In the future, studies need to be conducted with different samples, especially the middle-aged population. In addition, an automated analysis system should be developed, as should methods Table 4. Correlations among parameters of multi-line kymography. Variable
1
2
3
4
1. 2. 3. 4.
—
–.307*** —
.398*** –.162* —
.225*** –.045 .728*** —
Opening LPD Closing LPD Oqi SIi
*p < .05. ***p < .001.
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for simultaneous recording of HSDI and aerodynamic or acoustic parameters. Furthermore, HSDI studies should be performed with samples of individuals with various laryngeal diseases.
Conclusion The present study provides the first information about age-related differences of longitudinal oscillatory characteristics of the vocal folds using HSDI. Young women frequently displayed longitudinal phase differences such as PA opening and AP closing, resulting in zipper-like vocal fold movements. The vibratory patterns seen in young women were quite different from those seen in older women, who displayed various longitudinal phase differences of opening and closing, which resembled the findings in young men and older men. Age-related differences of OqMLK and SIMLK were also observed. Clinicians should be aware of these findings so they will be able to distinguish normality from abnormality and avoid overdiagnosis. Opening and closing longitudinal phase differences, as well as OqMLK and SIMLK, might be used clinically to assess laryngeal resistance and the severity of dysphonia, respectively.
Acknowledgments This research was presented at the 8th International Conference on Voice Physiology and Biomechanics, Erlangen, Germany, 2012.
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