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Vocal fold strain and vocal pitch in singing:Radiographic observations of singers and nonsingers
Journal of Voice Vol. 12, No. 3. pp. 274-286 © 1998 SingularPublishingGroup, Inc.
Vocal Fold Strain and Vocal Pitch in Singing: Radiographic Observations of Singers and Nonsingers A a t t o S o n n i n e n a n d Pertti H u r m e Department of Communication, UniversiO, of Jyviisk3,1ii, Jyviisk3,1gi, Finland
Summary: The relationship between vocal fold strain and vocal pitch in singers and nonsingers singing a rising pitch series has been indirectly investigated by means of lateral radiographs. Nonsingers tend to exhibit more strain than singers. To standardize the degree of strain, an index of strain per semitone is proposed. The semitone strain indicates the average amount of strain per I semitone of pitch increase or decrease. The index has been shown to be affected by several factors: gender, singing training, singing technique, voice class, age, and status of muscle function. Observations suggest that similar groups of individuals occupy different positions on the stress-strain curve, indicated by their semitone strain values. Key Words: Vocal fold elongation--Strain--Pitch-Singing--Radiography.
The present study examines vocal fold strain and pitch in singers and nonsingers. Strain is calculated from measurements of laryngeal distances (especially vocal fold length) seen on lateral radiographs, taken when producing a rising series of sustained /a/ vowels. Pitch is a perceptual term often used in music. It is not as exact as F 0, but it is precise enough for musical purposes. Minute variations in F 0 are not significant for the purposes of the present study; it is well known that F 0 varies in singers when singing at a certain pitch. Therefore, the term pitch was chosen for this study rather than fundamental frequency (F0). Changes in vocal fold length can be measured in absolute values such as millimeters. However, it is often useful to employ a normalized measure of
elongation such as strain. Strain is the change in length divided by the original starting length of the vocal fold multiplied by 100. Vocal pitch is related to the longitudinal tension, "effective stiffness," and "effective mass" of the vocal folds, and in some degree to subglottic pressure (1). The ability for variation in pitch originated in phylogenetic evolution when the rigid cricothyroid articulation of the larynx became mobile (2). Hence, an effective external control of tension in the vocal folds by the cricothyroid (CT) and ancillary muscles became possible in addition to an internal control provided by the thyroarytenoid muscle (TA). Thus, a voice physiology question emerges: How are changes in pitch related to biomechanical and geometrical changes of the vocal folds? As late as 1937, Tarneaud asserted that the vocal ligaments are nonelastic (3). However, in 1940, highspeed motion pictures of the human vocal folds by Bell Laboratories (4) showed beyond dispute that the vocal folds were elongated in a series of rising pitch.
Accepted for publication April 12, 1997. Address correspondence and reprint requests to: Aatto Sonninen, Gummeruksenkatu 3 B, FIN--40100 Jyv~iskylti,Finland. email: [email protected]
274
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
Later, several researchers made measurements in living human subjects, confirming the findings of Bell Laboratories' high-speed motion pictures. Methods included photography/videography by means of indirect laryngoscopy (5-14) and lateral radiographs (15-27). On the whole, such measurements show that, especially for the modal register, the vocal folds are lengthened as pitch increases and shortened as pitch decreases. As the vocal folds are elongated in a rising pitch series, their thickness decreases, again especially in the modal register. In the falsetto register such a decrease is less pronounced (28-32). Thus, it is evident that changes in pitch are related to changes in the geometry of the vocal folds. However, the consequences of such changes for voice production have only recently aroused the serious attention of researchers ( 1). In 1954 Sonninen suggested that the nonlinearity of the elongation curve of the vocal folds may be related to register transition (15). In 1960, van den Berg (33) elaborated the conditions and characteristics of the various registers in terms of the properties of the vocal ligaments and vocal muscles. He stressed the importance of the longitudinal tension in the vocal ligaments and the longitudinal tension in the vocal muscles in relation to the main vocal registers. Yumoto, Kadota, and Kurokawa (34 p. 318) concluded that some "structural differences of the vocal fold, especially the relation between the body and cover, may occur after lengthening the vocal folds." The elongation curves typically have more or less clearly the shape of the stress-strain curve (35,36). According to studies with excised larynges by Harless as early as 1852 (37), the elongation of the vocal folds in phonation was maximally about 20%. Aiipour-Haghighi, Titze and Perlman (38 p. 230) consider that "at low strain (0-20%) the tension in the body of the vocal folds is primarily under active control of the vocalis muscle. At higher strain (> 20%), the passive component becomes significant, making the tension in the body more controllable by muscles outside of the vocal fold (e.g., the CT and the strap muscles)." To make comparison between individuals possible and to gain deeper insights into the intra- and in-
275
terindividual factors influencing strain and pitch, we propose to standardize strain by means of an index of strain per one semitone, calculated by dividing the range of vocal fold strain (SR) in percent, with the frequency range of phonation (FRP) in semitones. The semitone strain index (SSI) gives the amount of strain per one semitone. The aim of this study is to explore relation of vocal strain to vocal pitch in living subjects. The SSI is introduced for that purpose. New biomechanical measurements have been made from old radiographs (15-18) produced by female and male singers and nonsingers to illustrate the usefulness of the SSI. The general aim is to better understand the physical laws and causality of voice production. METHODS
In the years 1953-1959 the senior author (A.S.) collected high-quality lateral spot radiographs of the larynx from more than 100 adult subjects (singers and nonsingers) who phonated the vowel/aJ at given pitches. The selection of material and methods in the present study slightly differ from those reported in earlier publications (15-18,26). New subsets were formed (Table 1). The methods of measurement have been revised, the results are given in strain values (instead of absolute values), and the statistical analyses have been improved. On the whole, the reanalyses correlate well with the original measurements. The correlation of the original measurements (18) and the reanalysis in one singer is high, both in measurements of the sagittal position (simple linear correlation, r = .93) and the vertical position of the larynx (r = .99), indicating high reliability (p<.0001). During radiography the subjects stood, with their forehead touching a support. The jaw was not fixed, but the subjects phonated the vowel/a/, thereby standardizing to some extent the position of the mandible and larynx. Figure 1 shows the anatomical structures and the ossification/calcification centers of which an easily recognizable characteristic was used as a measurement point: M = the mandible, H = the hyoid bone, T = the thyroid cartilage, A = the arytenoid car-
In earlier publications other abbreviations have been used: A for M, B for H, C for T, a for A. According to our observations (26), variation of the distance from the posterior measurement point is larger when measured at the anterior recess of the laryngeal ventricle than at the T point. However, measurements were taken at the laryngeal ventricle only in the few cases where the T point was not visible. Journal of Voice, Vol. 12, No. 3, 1998
276
AATTO SONNINEN AND PERTTI HURME T A B L E 1. Subjects (n = 67), their age, voice t3,pe, and voice range (~fknown) Number
NONSINGERS Females (FN) Subset I (FN) Older Younger Subset 2 (FN) Subset 3 (FN) Males (MN)
57 50 30 15 15 19 15 7
SINGERS Females (FS) MH KS MV EP RA IR HN Males (MS) AK JH LS
I0 7 47 40 65
Age
Voice type
Voice range
43 Soprano 41 Soprano 38 Mezzo-soprano 42
Soprano G#3-A6 Soprano C#3-G#6 Soprano D#3-C6 Mezzo-soprano
G#3-D6
34 Tenor Baritone
Tenor F2-A#4 D2-A4
G2-E5
16-70 16-66 x = 51, s = 3 x = 30, s = 8 x = 41, s =11 25-65
D#3-F6 C3-G#5
3 46 70
tilage, and C = the cricoid cartilage, i The points are indicated with the centers of small, unfilled circles. Naturally, such measurement points do not give an absolutely correct measure of the length of the vocal folds; they only give indirect information. These centers are visible in individuals below the age of 20 as small patches only, but with age they become enlarged and polymorphic. Ossification centers can be seen, for example, in the figures by Welch, Sergeant, and MacCurtain (39), Luchsinger (40 p 223) and Fyfe and Naylor (41). The technique of measuring vocal fold length by means of lateral radiographs is described in detail in earlier publications (15-18,26). More than 40 years have passed without anyone else extensively using this method. One reason for that may be the remark by Zenker and Zenker (42 p 6), suggesting that such methods are unreliable. This claim is valid if just a few subjects are examined. When measuring the length changes in vocal folds, the anterior-inferior part of thyroid cartilage was chosen to represent the anterior insertion (point T, visible in 58% of cases in adults) of the vocal folds (16). The posterior superior part of cricoid cartilage (point C, visible in 41% of Joun~al of Voice, Vol. 12, No. 3, 1998
D3-C6
Y
7I
FIG. 1. Schematicized anatomical structures as seen in lateral radiographs; measurement points shown in mandible (M), hyoid bone (H), thyroid (T), arytenoid (A), and cricoid cartilage (C). The procedure of measuring the position of point C (the ossification center of the cricoid cartilage) in relation to the 6th cervical vertebra (x: sagittal direction; y: vertical direction) is shown.
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
cases in adults) was chosen to represent the posterior insertion point of the vocal folds in all cases selected for this study. The ossification center of the arytenoid cartilage (point A) can seldom be seen in male subjects but can clearly be seen in 15 female nonsingers (Subset 3 in Table 1). The nonsinger group (n = 57; Table 1) consists of 50 female (FN) and 7 male (MN) nonsingers. This group does not consist of strictly normal subjects, but of goiter patients examined 2 to 4 days before thyroidectomy. No cases with pathological changes in the larynx, except for the possible effects of goiter (43), were included: All had healthy vocal folds free of pathology. Two subsets were chosen from the female nonsinger group. Subset 1 consisted of 30 female nonsingers. The older subjects comprised cases 1-15 and the younger subjects made up cases 16-30. The average ages in the groups were 51 and 30, respectively. Subset 2 consisted of 19 female nonsingers, who fulfilled several conditions: The pretracheal muscles (sternothyroid and hyothyroid, ST and HT) were bilaterally severed,2 they were x-rayed before the operation and within 3 weeks of the operation, and the length of their vocal folds could be measured from the T-C points describing the thyroid-cricoid distance (Fig. 1). Radiographic measurements of laryngeal distances, as well physiological voice range, were compared before and after thyroidectomy. There were no signs of laryngeal pathology. There was no noticeable change in general health (medically examined), vital capacity, or maximal duration of phonation before and after the operation. The singer group (n = I 0) consisted of 7 females (5 sopranos and 2 mezzo-sopranos) and 3 males (2 tenors and one baritone). All singers were found to be healthy by medical examination. Results from this material have been reported in several previous publications ( 17,18,26). The measurements on which this study is based concern vocal fold elongation in subjects phonating at certain pitches. To make comparison of subjects possible while maintaining the elongation pattern, the measurements were standardized to strain percentages. However, the choice of a reference level
277
may be problematic (44); the question will be discussed below. The task for the subjects was to sustain/a/vowels during radiography in as many pitches as possible out of seven given pitches (D#3, G#3, D#4, G#4, C5, D#5, and G#5). Notes at the chosen pitches were played on a piano and the subject imitated them as best as he or she could. In a subsample of 50 female nonsingers, the actual range measured during radiography was, on the average, about 88% of the total pitch range. Consequently, radiographs of the lowest and highest pitches of the physiological voice range are not available. In the present material a rest position (e.g., in quiet breathing) was seldom measured. The elongation values at D#4 (311 Hz), near the modal-falsetto transition, were used as the reference. These values are available for both female and male subjects. With D#4 in the middle of individual frequency ranges of phonation, the strain changes in low and high frequencies are better revealed. The strain values obtained from the measurements are influenced by methodological decisions: The technique of measurement (photography vs radiography) and the choice of the reference level can accentuate or disguise the differences between subjects. For comparison, in Figure 2 we summarize results by Hollien and Moore (5), who investigated vocal fold length in male nonsingers by photographic methods. In general, their data shows that vocal fold length in millimeters increases up to a certain pitch and then decreases. The point at which the voices of their subjects change from a low register to the falsetto is shown with an asterisk (above which a thinner line indicates the length of the vocal folds). In two subjects the voice changes to the falsetto at A3, in one subject at C4, and in three subjects at E4. The C4--E4 area largely corresponds to secondo passaggio in males (26). The general pattern of the data is that vocal fold length becomes shorter at higher pitches. On the average, the vocal folds appear to elongate until about the register transition area; above that area the vocal folds seem to be shortened. Similar results have been obtained in a previous study (8).
2 The operation naturally concludes with suturement. Journal of Voice, Vol. 12, No. 3, 1998
278
AATTO SONNINEN AND PERTTI HURME
• A Bass D Tenor
[] B B a r i t o n e
o C Baritone
• E Tenor
x F Tenor Falsetto
Low register 22 20 18
12 lO 8
25 J
E2 A2 C3 E3 A3 C4 E4 '
•
'
'
'
'
'
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'
20
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5 0 " E3 A3 C4 E4 A4 C5 E5 C3
~A.
0
• A Bass
-5 -10 O~ -15 • ~ -20 ~ -25 r.~ -30
The data can be interpreted in several ways, depending on the choice of reference level. Fig. 2 (second, third, and fourth panels) shows the effect of the choice of pitch as the reference level when converting millimeters to strain values in percent. The panels in the middle show strain values for subject A with E2 and E3 as the reference. The lowest panel shows strain values for all subjects with E4 as the reference (E4 was the note closest to the D#4 reference used in the present study). The conversion of elongation measures to strain percentages eliminates absolute measurements but maintains the shape and proportions of the pitch-length curve. The Hollien and Moore data can be described by the SSI by dividing SR (in percent) by FRP (in semitones): Case A (bass) 28.7/30 = .96, B (baritone) 42.0/37 = 1.14, C (baritone) 50.6,32 = 1.58, D (tenor) 29.3/20 = 1.47, E (tenor) 58.4/25 = 2.33, F (tenor) 60.7/28 = 2.17; the average for all is = 1.61. Generally, SSI is larger in tenors than in baritones and basses. The Hollien and Moore data illustrate the problems encountered in interpreting strain measurements. SR can be measured by the difference of the strain percent at the highest and lowest pitch if changes in strain are monotonic. Our measurements usually showed monotonic changes in strain. However, if the changes in strain were not monotonic, the difference between maximum and minimum strain values was chosen to indicate SR, regardless of the location of the maximum on the frequency scale. In some cases we also measured strain in different portions of the pitch range to obtain more detailed information on the behavior of the vocal folds.
-35 E2 A2 C 3 ~ A 3
C4
E4 A4 C5 E5
RESULTS 30 20
l0
i
0
-20 -30 -40 E2 A2
C3
E3 A3 C 4 ~
A4 C5
E5
F I G . 2. T h e effect o f choice o f reference level on strain values in percent, with the data from Hollien and M o o r e (5).
Journal ofVoice, Vol. 12, No. 3, 1998
Figure 3 illustrates the relationship of vocal fold strain and vocal pitch in each individual, separately for female and male singers and nonsingers (female nonsingers being represented by Subset 1). The SR for each individual is computed by subtracting the lowest strain percentage from the highest strain percentage. Strain percentages have been computed using the reference pitch of D#4. The same low pitch for various individuals in Fig. 3 may seem surprising. The explanation is that the FRP in semitones seen in this figure do not represent the subjects' physiologi-
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
P i t c h r a n g e (FRP) E2
D3
C4 A#4 G#5 F#6
279
m
P i t c h r a n g e (FRP)
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I
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;,n=7 i
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FIG. 3. Strain range (SR, gray areas) and the frequency range of phonation (FRP, horizontal bars) in female and male singers and nonsingers (FS, MS, FN, MN; Subset 1 in female nonsingers).
cal ranges, but only the range that was sung during radiography. From these values, average SR has been calculated for female and male singers and nonsingers. Typical strain values are below 20%. The dots in Figure 4 show the strain percentages calculated from measurements taken from radiographs; each x-ray is represented by one dot. The results are shown for female and male singers and nonsingers at all measured pitches. Strain percentages have been computed with the reference strain at D#4. The panels show the data points and average curves, calculated in pitch groups of 4 semitones. Linear regression lines describing the curves are steepest in female nonsingers (.64) and most level in male singers (.35). In male nonsingers the line is steeper than in female singers (.60 vs .50). To illustrate the relationship of curves describing strain percentage across pitch and the SSI, Figure 5 reproduces the curves for the female singers (n = 7). SSI values reflect the steepness of the strain-pitch curve.
On the whole, the curves are monotonic. At high pitches, the curves often level out. This is seen more clearly in Fig. 6, which gives the average strain percentage across pitch for each group. Figure 6 presents the average strain curves for female nonsingers and singers as well as male singers and nonsingers superimposed with the strain value at D4¢4 as the reference. The curves for males appear almost linear, even at the highest pitches, whereas the curve for female singers (and to some extent female nonsingers) resemble typical nonlinear stress-strain curves (1,36). At low pitches, women show a steeper increase in strain than men, whereas at midpitches the strain curves are practically identical for female and male subjects, which partly depends on the location of the reference strain. In high pitches, female subjects reach a higher strain percentage than male subjects. In all, female subjects have a wider range of strain than male subjects (about 20% vs about 15%). Journal of Voice, Vol. 12, No. 3, 1998
280
AATTO SONNINEN AND P E R T H HURME
M a l e s i n g e r s (n = 3) 15
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F e m a l e n o n s i n g e r s (n = 50)
F e m a l e s i n g e r s (n = 7)
5
i ,:
C6
C7
.._. C2
Z_~_ C3
C4
.. s 5 1 . 7 ; . C5
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Strain % 10
MS
..................
5
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0 F e m a l e s i n g e r s (n = 7) 15
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MH .43
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FIG. 5. The original vocal fold strain curves in female singers, with the SSI of each singer.
Journal of Voice, Vol. 12, No. 3, 1998
-15 -20
,
+
b
L
i
,
C2
C3
C4
C5
C6
C7
FIG. 6. Averaged frequency-strain curves for male nonsingers (MN), male singers (MS), female nonsingers (FN) and female singers (FS), adopted from Fig. 4. The curves have been superimposed with D#4 as the reference.
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
We present results below on the relation of the SSI and gender, age, voice training, and severing pretracheal muscles during thyroidectomy. Results pertaining to the measurement principle will also be presented.
Gender and training The measurements permit the comparison of female and male singers and nonsingers. The SSI (Fig. 4) is higher in nonsingers than singers: .58 in male singers, .63 in male nonsingers, .56 in female singers, and .72 in female nonsingers. However, the differences between the groups are not statistically significant. Figure 7 describes the frequency distribution of semitone strain indices calculated for female and male singers and nonsingers and in comparison for the Hollien and Moore (5) data. SSIs have been assigned to 20 categories from .25 to 2.15 at intervals of. 1. The columns indicate the number of subjects at each SSI. SSIs calculated from photographic data are higher (1.05-2.25) than from radiographic data (.25-1.55). In our data, males do not have SSIs higher than .95, whereas females show SSIs up to 1.45. Singers do not have SSIs higher than .85, whereas nonsingers show variation from .25 to 1.45. In sum, nonsingers used more strain (elongation) per one
281
semitone than singers and females used more strain (elongation) per one semitone than males. A more detailed analysis of one singer (EE Table 1), who sang a wide pitch range (each semitone up to G#6), allows the separate examination of two portions of the pitch range. In the lower portion ( - A # 4 ) the semitone strain index (based on the measurements of the T - A distance) is .81, but in the higher portion ( B 4 - ) the semitone strain is .29. The difference is statistically highly significant (p<.0001). Thus, as high pitch generally requires more stiffness (e.g., in EMG studies high pitches have been shown to be accompanied by high activity in the CT muscle), high SSI values may indicate low stiffness and low SSI values may indicate high stiffness in the vocal folds. This result is supported by stress-strain experiments (35,36). However, the activity of the TA muscle makes the relationship between stiffness and pitch more complicated, as discussed below.
Age hows the strain range in two groups of female nonsingers (Subset 1 in Table 1): the older subjects (cases 1-15; average age 51 years) and the younger subjects (cases 16-30; average age 30 years). The average
Subjects 14 12 10 8 6 4 2 0 tr~ ¢-,I
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FIG. 7. The frequency distribution of semitone strain indices calculated for female and male singers and nonsingers (FS, MS, FN, MN) and for the Hollien and Moore data (H-M) (5). Journal of Voice, Vol. 12, No. 3, 1998
282
AATTO SONNINEN AND PERTTI HURME
FRP was significantly narrower in the older group (16 semitones) than in the younger group (21 semitones; p<.0057). The strain curve as described by linear regression is less steep (.44) in the older group than in the younger group (.77). The younger subjects show especially low strain values at lowest pitches (which the older subjects could not sing). , Figure 9 describes the frequency distribution of semitone strain indices calculated for the older and younger subjects. The SSI is significantly lower in the older group (.57) than in the younger group (.96; p< .0009). The simple linear correlation between SSI and age is significant (p<.0011). Other correlations (e.g., between age and highest note produced or strain percentage, or between strain and highest note produced or frequency range of phonation), were not significant. It can be concluded that younger female nonsingers exhibited more strain (elongation of vocal folds) per one semitone than older nonsingers.
Thyroideetomy The effect of bilaterally severing pretracheal muscles is examined by means of the semitone strain index in 19 cases of female nonsingers before and after thyroidectomy (Figure 10, Subset 2 in Table I). The correlation between the difference between the highest musical tone in semitones (HMT) before and after the operation with difference between SSI before and after the operation is almost significant (p< .02). The preoperational average of SSI is .76 and the postoperational average is.64. Thus, strain per one semitone was slightly smaller after bilaterally severing pretracheal muscles. Described by linear regression, the strain curve is less steep (.48) after the operation than before (.66).
F e m a l e n o n s i n g e r s (n = 30) • O l d e r subjects
[] Y o u n g e r subjects
15, 10. 5 0
T
".
-5
.
-10 rJ3 -15 -20 -25 -30 D#3
D#4
A#5
FIG. 8. Averaged strain curves and standard deviations in two groups of female nonsingers (Subset I): the older subjects (cases 1-15) and the younger subjects (cases 16-30).
Subjects 5 4 3 2 1 0
[--] Y o u n g e r
tr3 o-4
m
~
m
~
SSI
FIG. 9. The frequency distribution of semitone strain indices calculated for the older and younger subjects (Subset 1, n = 30).
Subjects
Method of measurement Figure 11 shows the strain percentages in the female nonsingers, where both T-C and T - A measurements could be taken (n = 15, Subset 3 in Table 1). The SSI values calculated from both measurements are also shown. In general, the indexes from T - A measurements are larger than from T-C measurements: .95 vs..73. A comparison of vocal fold strain ranges shows that the values closer to the actual strain values (T-A, 16.4%) are about 30% larger than those indicated by the T-C measurements (12.7%). Journal ofVoice, Vol. 12, No. 3, 1998
0 . . . . . . .
m
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tn
:11: :11:11: : m
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FIG. 10. The frequency distribution of semitone strain indices calculated for female nonsingers (Subset 2) before and after thyroidectomy.
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
F e m a l e n o n s i n g e r s (n = 15) --T-C
T-A
15 I(1
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.69 .72 1.09 1.00
.83 .84 .86 .93 1.00 1.09T-C .50 1.06 1.04 1.48 1.40 1.18 T-A
FIG. 11. The strain curves in the female nonsingers in which both T - C and T - A measurements could be taken. The SSI calculated from both measurements are also shown.
DISCUSSION The SSI calculated from T - A measurements probably better reflects the "real" movements of vocal folds, but unfortunately, there is more risk for measurement errors as the calcification points in the arytenoids are not always as clearly visible as in the cricoid cartilage. Therefore, we have to content ourselves with T-C, even though T - A would have been a better measure. The ability of the subjects (especially nonsingers) to sing at various pitches varied greatly: some were able to sing at three pitches and some were able to sing at seven pitches. Such differences decrease the reliability of the SSI. When calculating the value of the SSI, the choice of the reference length of the vocal folds is crucial. Here, the length at D#4 in millimeters was used. First, SSI was calculated for each individual by dividing the SR by the FRP. Group averages were then calculated from the individual SSIs. Group averages can be different (and less sensitive to individual variation) if the group average of strain range is divided by the group average of FRP.
283
Changes in strain with pitch were generally monotonic. However, vocal folds were not always smoothly elongated; occasionally, rather abrupt length adjustments (including shortening) were observed. It is evident that the reliability of the results is affected by the number of measurements taken. The division of the pitch range into portions with their own SSI also increases the accuracy of SSI. The results presented above are based on the assumption that the use of the reference level (the individual distance of T-C in millimeters when singing D#4 in the present study) is a valid method. Other levels of reference have been proposed, e.g., minimum length, length during respiration, and length during transcutaneous electrical stimulation of the recurrent laryngeal nerve (13). Such measures are, in our opinion, not superior to the method employed in the present study. With the reference level at D#4, elongation variation was standardized in relation to the T - A or T-C distance. The laryngeal behavior of individuals was examined on this basis. Theoretically, it is possible for stress or strain to be chosen as an independent variable. If strain is the independent variable, we are in accord with the following statement by Titze ( 1 p 42): "for equal longitudinal strain [italics ours] applied to the vocal folds, the greatest stress is developed in the epithelium, then in the ligament, and then in the thyroarytenoid muscle" The differences between the curves are due to differences in the extensibility of the layers. From the point of view of biomechanics and physiology, however, strain and pitch are dependent and stress (equaling external forces stretching the vocal folds) is always independent. There are anatomically and physiologically differing layers in the vocal folds (45). When a certain amount of external longitudinal stress (force) is applied to the epithelium or ligament (cover), the strain is relatively low compared to the strain of the muscle for the same amount of passive stress. Such is the case when the muscle is passive; if the body is activated, the situation can be the opposite: The strain of the body is less than the strain of the cover (36). According to Hirano (36), external stretching forces increase stress both in the cover and body, and internal contraction (in TA) increases stress in the body and decreases stress in cover layer. Consequently, the thyroarytenoid muscle regulates whether Journal of Voice, 'CoL 12, No. 3, 1998
284
AATTO SONNINEN AND PERTTI HURME
the body or the cover has greater stress (with constant external stress). This is in line with the hypothesis that the balancing (relative stiffening) of the body of the vocal fold with respect to the cover, and vice versa, is a major factor in pitch and register control in the voice (1,46). Therefore, a low SSI value does not always indicate greater stiffness than a high SSI value. Even if two individuals have the same SSI value, "they can differ in the stiffness of their vocal folds. When investigating vocal folds in living human beings, both strain and pitch are also determined by the stress of laryngeal muscles. The strain of the vocal folds can be relatively easily measured (if the ossification centers are visible in radiography). On the other hand, it is extremely difficult or even impossible at the present time to directly measure stress in a living human being (47). As stress values are not available. a range of pitch variation replaces stress and strain is examined at various pitches. Is the SSI useful? The curves describing strain and vocal pitch are nonlinear and resemble stress-strain curves (Fig. 4). In singing, the SSI is smaller in high pitch than in low pitch, probably indicating that stress (and possibly stiffness) has a high level in high vocal pitch and a low level in low pitch. Male subjects and singers have a lower semitone strain index (possibly indicating more stiffness) and female subjects and nonsingers have a higher index (possibly indicating less stiffness). The interpretation presented above is that low SSI indicates high inner stress and high SSI indicates low inner stress. This view receives tentative support from our observations; however, the contribution of the activity of the TA muscle complicates the relationship. Higher age is associated with lower semitone strain. In older individuals the connective tissue of the vocal folds can become stiffer ("fibrosis" of connective tissue, 48) and the stretching stress of external muscles weaker. In Fig. 8 the basic difference between the subjects can be seen only for the lowest pitch group, which is missing for the older subjects. The higher SSI of the younger subjects may thus be based on the way the semitone strain was calculated. Or could it be possible that stiffer vocal folds make it more difficult for the older subjects to sing the lowest tones? Titze (49) suggests that higher pitch in females is due to more stiffness and less elongation than in males. However, Fig. 6 shows that SSI is smaller and Journal of Voice, Vol. 12, No. 3, 1998
the stress-strain curve more linear for males than females, indicating that vocal fold tissue may be slightly stiffer in males than in females. This may be explained by the greater percentage of collagenous fibers in male than female vocal folds (48). However, it is clear that further comparative studies of the histological and microdynamic structure are needed. Is stiffness of tissue one of the factors accounting for differences between bass and tenor singers? Nonsingers use much strain to achieve their relatively narrow FRP, whereas singers use less strain and perhaps reduce the vibrating mass in accordance with the spring model: "to double the frequency of vibration, the m a s s . . , may be reduced to one-fourth its original size, or the spring constant . . . may be made four times larger" (50 p 20). The trained singer can relax the vocal muscle by means of "covering," whereby the cover of the vocal folds becomes stiffer. CONCLUSIONS i. The relationship between vocal fold strain and vocal pitch in singing a rising pitch series is described by the SSI which indicates standardized elongation of vocal folds by means of an average of vocal fold strain per one semitone. SSI is calculated by dividing the SR in percent by the FRP in semitones. 2. The relationship between vocal fold strain and vocal pitch is nonlinear and follows the stress-strain curve of organic tissue. 3. The SSI is influenced by structural and functional factors. Structural factors include: a) gender (SSI is higher in female than male subjects), b) age (SSI is higher in younger than older subjects), and c) organic insufficiency of strap muscles (SSI is lower after thyroidectomy than before the operation). The observed differences (which may indicate differences in stiffness) may be explained by the greater percentage of collagenous fibers and other connective tissue in males and in older subjects than in females and younger subjects. Functional factors include: (a) pitch placement (at lower pitches the SSI is higher than at higher pitches) and (b) vocal training (SSI is higher in nonsingers than singers). 4. Low SSI generally indicates much stiffness and high SSI indicates little stiffness in the vocal folds. However, even in cases where SSI is similar, there can be large differences in effective stiffness. Such differ-
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
ences may be due to variation in the structure of vocal fold tissue and to variation in the activity of the TA muscle. Measurements of a female singer singing a rising pitch series in semitone steps (to be reported by the present authors in a forthcoming publication) show that even when SSI remains about constant, greater effective stiffness in the vocal folds is manifested by typical changes in external laryngeal distances. 5. The SSI is a delicate measure. Because they are located between the thyroid cartilage and the arytenoid cartilages, the vocal folds cannot be directly measured in living human beings either by photography or by radiography. Sources of error in photography include the pulling of the tongue, the insertion of a mirror in the oropharynx, projection errors, and possibly the contraction of the laryngeal aditus (especially in higher pitches). It is also difficult to determine the exact point of measurement in the mucosa when using photographic methods. However, radiographic measurements also have problems. The risk of overexposure to radiation limits the use of the method on healthy subjects. The doses used in this study (where the material was collected 40 years ago) were low, with 100 exposures on the neck area corresponding to one exposure habitually used on the pelvic area. Radiographic methods are also hampered by the difficulty of selecting suitable subjects, as the ossification points are clearly visible in only about half of them. The radiographic measurements reported in this study are from the T-C distances. The results would be different if it had been possible to take T-A measurements, which better reflect the length of the vocal folds for all subjects. 6. Further studies exploring the factors that affect the SSI are needed to standardize the measurement procedure and to evaluate the significance of SSI.
Acknowledgments: We wish to thank Dr. Ronald Baken and three anonymous reviewers for their critical and constructive comments on an earlier version of this article. We are also grateful to Drs. Johan Sundberg, Erkki Vilkman, Anne-Maria Laukkanen, and Paavo Malinen for fruitful discussions.
REFERENCES 1. Titze IR. Principles of Voice Production. Englewood Cliffs, N J: Prentice-Hall; 1994.
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2. Negus VE. The Comparative Anatomy and Physiology of the /-xtl3,n-r. London: William Heinemann; 1949. 3. Tameaud J. Die Stimmlippen im Zustande der Phonation. Hals-, Nasen- u. Ohrenarzt 1937;28:36-48. 4. Farnsworth DW. High-speed motion pictures of the human vocal cords. Bell l_xlboratories Record 1940; 18:203-8. 5. Hollien H, Moore P. Measurements of the vocal folds during changes in pitch. J Speech Hear Res 1960;3:157-65. 6. Pfau W. Diskussionbeitrag zum Vortrag von Prof. Dr. Luchsinger. Kongtessbericht der Gemeinschaftstagung fiir allgemeinen und angewandte Phonetik. Hamburg: 1960:60. 7. Pfau W. Zur Frage der Stimmlippenverl~ingerung beim Aufwtirtssingen. Archiv Ohr- usw. Heilk. a. Z. Hals- tts~ Heilk 1961 ; 177:458-66. 8. Luchsinger R, Pfister K. Die Messung der Stimmlippenverl~ingemng beim Steigem der Tonhfhe. Folia Phoniatr 1961: 13(I):1-12. 9. Wendler J. Messung der Stimmlippenlfinge. Z l_xtl3,ngol Rhinol 1965;'44:162-73. I 0. Wendler J. Stimmlippenlfinge und Tonhfhe. Z l_xtt3'ngol Rhinol 1966;45:355-69. I 1. Hollien H, Brown W Jr, Hollien K. Vocal fold length associated with modal, falsetto and varying intensity phonation. Folia Phoniatr 1971 ;23:66-78. 12. Hollien H. Three major vocal registers: a proposal. In: Rigault A, Charbonneau R, eds. Ptvceedings of the 7th htternational Congress of Phonetic Sciences. The Hague: Mouton; 1972:320-3 I. 13. Nishizawa N, Sawashima M, Yonemoto K. Vocal fold length in vocal pitch change. In: Fujimura O, ed. Vocal Physiology: Voice Production, Mechanisms and Functions. New York, NY: Raven Press; 1988:75-82. 14. Lindestad P-/~, Stidersten M. Laryngeal and pharyngeal behavior in countertenor and baritone singing--a videofiberscopic study. J Voice 1988;2(2):132-9. 15. Sonninen A. ls the length of vocal cords the same at all different levels of singing? Acta Otolal3'ngol S,ppl 1954;11 : 219-31. 16. Sonninen A. The role of the external laryngeal muscles in length-adjustment of the vocal cords in singing, Acta Otolal3'ngol Suppl 1956; 130. 17. Sonninen A. Paratasisgram of the vocal cords and the dimensions of the voice. In: Sovijfirvi A, ed. Proceedings of the 4th hztenlational Congress of Phonetic Sciences. Helsinki: Mouton; 1962:250-8; also in: Large J, ed. Contributions of Voice Resealz'h to Singing. Houston, TX: College-Hill Press; 1980: 134-45. 18. Sonninen A. The external frame function in the control of pitch in the human voice. Ann NYAcad Sci 1968;155:68-90. 19. Hollien H. Some laryngeal correlates of vocal pitch. J Speech Heat" Res 1960a;3:52-8. 20. Hollien H. Vocal pitch variation related to changes in vocal fold length. J Speech Hear Res 1960b;3:150-6. 21. Hollien H. On vocal registers. J Phonet 1974;2:125-43. 22. Damst6 PH. X-ray study of vocal fold length. Folia Phoniatr
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23. Damst6 PH, Hollien H, Moore E Murry T. An x-ray study of vocal fold length. Folia Phoniatr 1968;20(6):349-59. 24. Hollien H, Damst6 PH, Murry T. Vocal fold length during vocal fry phonation. Folia Phoniatr 1969;21 (4):257--65. 25. Run W, Chung Y. Roentgenological measurement of physiological vocal cord length. Folia Phoniatr 1983;353:289-93. 26. Sonninen A. Hurrne, E Vilkman E. Roentgenological observations on vocal fold length-changes with special reference to register transition and open/covered voice. Scand J Log Phon 1992;17:95-106. 27. Hertegfird S, Hgtkansson A, Thorstensen 13 Vocal fold length measurements with computed tomography. Scand J Log Phon 1993;19(2-3):57-63. 28. Hollien H, Curtis JF. A laminagraphic study of vocal pitch. J Speech Heat" Res 1960;3:363-7 I. 29. Hollien H. The relationship of vocal fold thickness and fundamental frequency of phonation. J Speech Heat" Res 1962; 5:237--43. 30. Hollien H, Colton RH. Four laminagraphic studies of vocal fold thickness. Folia Phoniatr 1969;21 : 179-95. 31. Hollien H, Coleman RF. Laryngeal correlates of frequency change: a STROL study. J Speech Hear Res 1970;13(2): 271-8. 32. Allen EL, Hollien H. Vocal fold thickness in the pulse (vocal fry) register. Folia Phoniatr 1973;25:241-50. 33. van den Berg JW. Vocal ligaments versus registers. In: Trojan F, ed. Current Problems hi Phoniatrics amt Logopedics. Basel: Karger; 1960:19-34. 34. Yumoto E, Kadota Y, Kurokawa H. Infraglottic aspect of canine vocal fold vibration: effect of increase of mean airflow rate and lengthening of vocal fold. J Voice 1993; 7(4): 311-8. 35. Sonninen A, Damst6 PH, Jol J, Fokkens J, Roelofs J. Microdynamics in vocal fold vibration. Acta Otolao,ngol 1974; 78:129-34. 36. Hirano M. Phonosurgery basic and clinical investigations. Otologia (Fukuoka) Suppl 1975; 1:21.
Journal of Voice, Vol. 12, No. 3, 1998
37. Harless 1852, quoted by Tarneaud 1937:39 and Panconcelli-Calzia G. 3000 Jahre Stimmforschung. Marburg: Elwert; 1961:38. 38. Alipour-Haghighi F, Titze IR, Perlman AL. Tetanic contraction in vocal fold muscle. J Speech Heat" Res 1989;32: 226-3 I. 39. Welch G, Sergeant D, MacCurtain E Some physical characteristics of the male falsetto voice. J Voice 1988;2(2): 151-63. 40. Luchsinger R. In: Luchsinger R, Arnold GE, eds. VoiceSpeech-l_zmguage. Belmont, Calif: Wadsworth; 1965:3-334. 41. Fyfe F, Naylor E. Calcification and ossification in the cricoid cartilage of the larynx, with notation on the mechanism of change of pitch. Proc Can Otolar Soc 1958:67-79. 42. Zenker W, Zenker A. Uber die Regelung der Stimmlippenspannung durch von aussen eingreifenden Mechanismen. Folia Phoniatr 1960; 12:1-136. 43. Sonninen A. Laryngeal signs and symptoms of goitre. Folia Phoniatr 1960; 12:41-7. 44. Colton RH. Physiological mechanisms of vocal frequency control: the role of tension, J Voice 1988;2(3):208-20. 45. Kahane JC. Histologic structure and properties of the human vocal folds. Eat-Nose Throat J 1988;67;322-30. 46. Hirano M. Structure and vibratory behavior of the vocal folds. In: Sawashima M, Cooper F, eds. Dynamic Aspects of Speech Pl~gduction. Tokyo: University of Tokyo; 1977: 13-30. 47. Kitajima K, Tanaka T. Effects of intraoral pressure change on F0 regulation--preliminary study for the evaluation of vocal fold stiffness. J Voice 1995;9(4):424-8. 48. Kahane JC. Connective tissue changes in the larynx and their effects on voice. J Voice 1987; I ( I ):27-30. 49. Titze IR. Physiologic and acoustic differences between male and female voices. J Acous Soc Am 1989;85(4): 1699-707. 50. Rossing TD. The Science of Sound. 2nd ed. Reading, MA: Addison-Wesley; 1990.
Vocal Fold Strain and Vocal Pitch in Singing: Radiographic Observations of Singers and Nonsingers A a t t o S o n n i n e n a n d Pertti H u r m e Department of Communication, UniversiO, of Jyviisk3,1ii, Jyviisk3,1gi, Finland
Summary: The relationship between vocal fold strain and vocal pitch in singers and nonsingers singing a rising pitch series has been indirectly investigated by means of lateral radiographs. Nonsingers tend to exhibit more strain than singers. To standardize the degree of strain, an index of strain per semitone is proposed. The semitone strain indicates the average amount of strain per I semitone of pitch increase or decrease. The index has been shown to be affected by several factors: gender, singing training, singing technique, voice class, age, and status of muscle function. Observations suggest that similar groups of individuals occupy different positions on the stress-strain curve, indicated by their semitone strain values. Key Words: Vocal fold elongation--Strain--Pitch-Singing--Radiography.
The present study examines vocal fold strain and pitch in singers and nonsingers. Strain is calculated from measurements of laryngeal distances (especially vocal fold length) seen on lateral radiographs, taken when producing a rising series of sustained /a/ vowels. Pitch is a perceptual term often used in music. It is not as exact as F 0, but it is precise enough for musical purposes. Minute variations in F 0 are not significant for the purposes of the present study; it is well known that F 0 varies in singers when singing at a certain pitch. Therefore, the term pitch was chosen for this study rather than fundamental frequency (F0). Changes in vocal fold length can be measured in absolute values such as millimeters. However, it is often useful to employ a normalized measure of
elongation such as strain. Strain is the change in length divided by the original starting length of the vocal fold multiplied by 100. Vocal pitch is related to the longitudinal tension, "effective stiffness," and "effective mass" of the vocal folds, and in some degree to subglottic pressure (1). The ability for variation in pitch originated in phylogenetic evolution when the rigid cricothyroid articulation of the larynx became mobile (2). Hence, an effective external control of tension in the vocal folds by the cricothyroid (CT) and ancillary muscles became possible in addition to an internal control provided by the thyroarytenoid muscle (TA). Thus, a voice physiology question emerges: How are changes in pitch related to biomechanical and geometrical changes of the vocal folds? As late as 1937, Tarneaud asserted that the vocal ligaments are nonelastic (3). However, in 1940, highspeed motion pictures of the human vocal folds by Bell Laboratories (4) showed beyond dispute that the vocal folds were elongated in a series of rising pitch.
Accepted for publication April 12, 1997. Address correspondence and reprint requests to: Aatto Sonninen, Gummeruksenkatu 3 B, FIN--40100 Jyv~iskylti,Finland. email: [email protected]
274
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
Later, several researchers made measurements in living human subjects, confirming the findings of Bell Laboratories' high-speed motion pictures. Methods included photography/videography by means of indirect laryngoscopy (5-14) and lateral radiographs (15-27). On the whole, such measurements show that, especially for the modal register, the vocal folds are lengthened as pitch increases and shortened as pitch decreases. As the vocal folds are elongated in a rising pitch series, their thickness decreases, again especially in the modal register. In the falsetto register such a decrease is less pronounced (28-32). Thus, it is evident that changes in pitch are related to changes in the geometry of the vocal folds. However, the consequences of such changes for voice production have only recently aroused the serious attention of researchers ( 1). In 1954 Sonninen suggested that the nonlinearity of the elongation curve of the vocal folds may be related to register transition (15). In 1960, van den Berg (33) elaborated the conditions and characteristics of the various registers in terms of the properties of the vocal ligaments and vocal muscles. He stressed the importance of the longitudinal tension in the vocal ligaments and the longitudinal tension in the vocal muscles in relation to the main vocal registers. Yumoto, Kadota, and Kurokawa (34 p. 318) concluded that some "structural differences of the vocal fold, especially the relation between the body and cover, may occur after lengthening the vocal folds." The elongation curves typically have more or less clearly the shape of the stress-strain curve (35,36). According to studies with excised larynges by Harless as early as 1852 (37), the elongation of the vocal folds in phonation was maximally about 20%. Aiipour-Haghighi, Titze and Perlman (38 p. 230) consider that "at low strain (0-20%) the tension in the body of the vocal folds is primarily under active control of the vocalis muscle. At higher strain (> 20%), the passive component becomes significant, making the tension in the body more controllable by muscles outside of the vocal fold (e.g., the CT and the strap muscles)." To make comparison between individuals possible and to gain deeper insights into the intra- and in-
275
terindividual factors influencing strain and pitch, we propose to standardize strain by means of an index of strain per one semitone, calculated by dividing the range of vocal fold strain (SR) in percent, with the frequency range of phonation (FRP) in semitones. The semitone strain index (SSI) gives the amount of strain per one semitone. The aim of this study is to explore relation of vocal strain to vocal pitch in living subjects. The SSI is introduced for that purpose. New biomechanical measurements have been made from old radiographs (15-18) produced by female and male singers and nonsingers to illustrate the usefulness of the SSI. The general aim is to better understand the physical laws and causality of voice production. METHODS
In the years 1953-1959 the senior author (A.S.) collected high-quality lateral spot radiographs of the larynx from more than 100 adult subjects (singers and nonsingers) who phonated the vowel/aJ at given pitches. The selection of material and methods in the present study slightly differ from those reported in earlier publications (15-18,26). New subsets were formed (Table 1). The methods of measurement have been revised, the results are given in strain values (instead of absolute values), and the statistical analyses have been improved. On the whole, the reanalyses correlate well with the original measurements. The correlation of the original measurements (18) and the reanalysis in one singer is high, both in measurements of the sagittal position (simple linear correlation, r = .93) and the vertical position of the larynx (r = .99), indicating high reliability (p<.0001). During radiography the subjects stood, with their forehead touching a support. The jaw was not fixed, but the subjects phonated the vowel/a/, thereby standardizing to some extent the position of the mandible and larynx. Figure 1 shows the anatomical structures and the ossification/calcification centers of which an easily recognizable characteristic was used as a measurement point: M = the mandible, H = the hyoid bone, T = the thyroid cartilage, A = the arytenoid car-
In earlier publications other abbreviations have been used: A for M, B for H, C for T, a for A. According to our observations (26), variation of the distance from the posterior measurement point is larger when measured at the anterior recess of the laryngeal ventricle than at the T point. However, measurements were taken at the laryngeal ventricle only in the few cases where the T point was not visible. Journal of Voice, Vol. 12, No. 3, 1998
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AATTO SONNINEN AND PERTTI HURME T A B L E 1. Subjects (n = 67), their age, voice t3,pe, and voice range (~fknown) Number
NONSINGERS Females (FN) Subset I (FN) Older Younger Subset 2 (FN) Subset 3 (FN) Males (MN)
57 50 30 15 15 19 15 7
SINGERS Females (FS) MH KS MV EP RA IR HN Males (MS) AK JH LS
I0 7 47 40 65
Age
Voice type
Voice range
43 Soprano 41 Soprano 38 Mezzo-soprano 42
Soprano G#3-A6 Soprano C#3-G#6 Soprano D#3-C6 Mezzo-soprano
G#3-D6
34 Tenor Baritone
Tenor F2-A#4 D2-A4
G2-E5
16-70 16-66 x = 51, s = 3 x = 30, s = 8 x = 41, s =11 25-65
D#3-F6 C3-G#5
3 46 70
tilage, and C = the cricoid cartilage, i The points are indicated with the centers of small, unfilled circles. Naturally, such measurement points do not give an absolutely correct measure of the length of the vocal folds; they only give indirect information. These centers are visible in individuals below the age of 20 as small patches only, but with age they become enlarged and polymorphic. Ossification centers can be seen, for example, in the figures by Welch, Sergeant, and MacCurtain (39), Luchsinger (40 p 223) and Fyfe and Naylor (41). The technique of measuring vocal fold length by means of lateral radiographs is described in detail in earlier publications (15-18,26). More than 40 years have passed without anyone else extensively using this method. One reason for that may be the remark by Zenker and Zenker (42 p 6), suggesting that such methods are unreliable. This claim is valid if just a few subjects are examined. When measuring the length changes in vocal folds, the anterior-inferior part of thyroid cartilage was chosen to represent the anterior insertion (point T, visible in 58% of cases in adults) of the vocal folds (16). The posterior superior part of cricoid cartilage (point C, visible in 41% of Joun~al of Voice, Vol. 12, No. 3, 1998
D3-C6
Y
7I
FIG. 1. Schematicized anatomical structures as seen in lateral radiographs; measurement points shown in mandible (M), hyoid bone (H), thyroid (T), arytenoid (A), and cricoid cartilage (C). The procedure of measuring the position of point C (the ossification center of the cricoid cartilage) in relation to the 6th cervical vertebra (x: sagittal direction; y: vertical direction) is shown.
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
cases in adults) was chosen to represent the posterior insertion point of the vocal folds in all cases selected for this study. The ossification center of the arytenoid cartilage (point A) can seldom be seen in male subjects but can clearly be seen in 15 female nonsingers (Subset 3 in Table 1). The nonsinger group (n = 57; Table 1) consists of 50 female (FN) and 7 male (MN) nonsingers. This group does not consist of strictly normal subjects, but of goiter patients examined 2 to 4 days before thyroidectomy. No cases with pathological changes in the larynx, except for the possible effects of goiter (43), were included: All had healthy vocal folds free of pathology. Two subsets were chosen from the female nonsinger group. Subset 1 consisted of 30 female nonsingers. The older subjects comprised cases 1-15 and the younger subjects made up cases 16-30. The average ages in the groups were 51 and 30, respectively. Subset 2 consisted of 19 female nonsingers, who fulfilled several conditions: The pretracheal muscles (sternothyroid and hyothyroid, ST and HT) were bilaterally severed,2 they were x-rayed before the operation and within 3 weeks of the operation, and the length of their vocal folds could be measured from the T-C points describing the thyroid-cricoid distance (Fig. 1). Radiographic measurements of laryngeal distances, as well physiological voice range, were compared before and after thyroidectomy. There were no signs of laryngeal pathology. There was no noticeable change in general health (medically examined), vital capacity, or maximal duration of phonation before and after the operation. The singer group (n = I 0) consisted of 7 females (5 sopranos and 2 mezzo-sopranos) and 3 males (2 tenors and one baritone). All singers were found to be healthy by medical examination. Results from this material have been reported in several previous publications ( 17,18,26). The measurements on which this study is based concern vocal fold elongation in subjects phonating at certain pitches. To make comparison of subjects possible while maintaining the elongation pattern, the measurements were standardized to strain percentages. However, the choice of a reference level
277
may be problematic (44); the question will be discussed below. The task for the subjects was to sustain/a/vowels during radiography in as many pitches as possible out of seven given pitches (D#3, G#3, D#4, G#4, C5, D#5, and G#5). Notes at the chosen pitches were played on a piano and the subject imitated them as best as he or she could. In a subsample of 50 female nonsingers, the actual range measured during radiography was, on the average, about 88% of the total pitch range. Consequently, radiographs of the lowest and highest pitches of the physiological voice range are not available. In the present material a rest position (e.g., in quiet breathing) was seldom measured. The elongation values at D#4 (311 Hz), near the modal-falsetto transition, were used as the reference. These values are available for both female and male subjects. With D#4 in the middle of individual frequency ranges of phonation, the strain changes in low and high frequencies are better revealed. The strain values obtained from the measurements are influenced by methodological decisions: The technique of measurement (photography vs radiography) and the choice of the reference level can accentuate or disguise the differences between subjects. For comparison, in Figure 2 we summarize results by Hollien and Moore (5), who investigated vocal fold length in male nonsingers by photographic methods. In general, their data shows that vocal fold length in millimeters increases up to a certain pitch and then decreases. The point at which the voices of their subjects change from a low register to the falsetto is shown with an asterisk (above which a thinner line indicates the length of the vocal folds). In two subjects the voice changes to the falsetto at A3, in one subject at C4, and in three subjects at E4. The C4--E4 area largely corresponds to secondo passaggio in males (26). The general pattern of the data is that vocal fold length becomes shorter at higher pitches. On the average, the vocal folds appear to elongate until about the register transition area; above that area the vocal folds seem to be shortened. Similar results have been obtained in a previous study (8).
2 The operation naturally concludes with suturement. Journal of Voice, Vol. 12, No. 3, 1998
278
AATTO SONNINEN AND PERTTI HURME
• A Bass D Tenor
[] B B a r i t o n e
o C Baritone
• E Tenor
x F Tenor Falsetto
Low register 22 20 18
12 lO 8
25 J
E2 A2 C3 E3 A3 C4 E4 '
•
'
'
'
'
'
A4 C5 E5 '
'
20
.~
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5 0 " E3 A3 C4 E4 A4 C5 E5 C3
~A.
0
• A Bass
-5 -10 O~ -15 • ~ -20 ~ -25 r.~ -30
The data can be interpreted in several ways, depending on the choice of reference level. Fig. 2 (second, third, and fourth panels) shows the effect of the choice of pitch as the reference level when converting millimeters to strain values in percent. The panels in the middle show strain values for subject A with E2 and E3 as the reference. The lowest panel shows strain values for all subjects with E4 as the reference (E4 was the note closest to the D#4 reference used in the present study). The conversion of elongation measures to strain percentages eliminates absolute measurements but maintains the shape and proportions of the pitch-length curve. The Hollien and Moore data can be described by the SSI by dividing SR (in percent) by FRP (in semitones): Case A (bass) 28.7/30 = .96, B (baritone) 42.0/37 = 1.14, C (baritone) 50.6,32 = 1.58, D (tenor) 29.3/20 = 1.47, E (tenor) 58.4/25 = 2.33, F (tenor) 60.7/28 = 2.17; the average for all is = 1.61. Generally, SSI is larger in tenors than in baritones and basses. The Hollien and Moore data illustrate the problems encountered in interpreting strain measurements. SR can be measured by the difference of the strain percent at the highest and lowest pitch if changes in strain are monotonic. Our measurements usually showed monotonic changes in strain. However, if the changes in strain were not monotonic, the difference between maximum and minimum strain values was chosen to indicate SR, regardless of the location of the maximum on the frequency scale. In some cases we also measured strain in different portions of the pitch range to obtain more detailed information on the behavior of the vocal folds.
-35 E2 A2 C 3 ~ A 3
C4
E4 A4 C5 E5
RESULTS 30 20
l0
i
0
-20 -30 -40 E2 A2
C3
E3 A3 C 4 ~
A4 C5
E5
F I G . 2. T h e effect o f choice o f reference level on strain values in percent, with the data from Hollien and M o o r e (5).
Journal ofVoice, Vol. 12, No. 3, 1998
Figure 3 illustrates the relationship of vocal fold strain and vocal pitch in each individual, separately for female and male singers and nonsingers (female nonsingers being represented by Subset 1). The SR for each individual is computed by subtracting the lowest strain percentage from the highest strain percentage. Strain percentages have been computed using the reference pitch of D#4. The same low pitch for various individuals in Fig. 3 may seem surprising. The explanation is that the FRP in semitones seen in this figure do not represent the subjects' physiologi-
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
P i t c h r a n g e (FRP) E2
D3
C4 A#4 G#5 F#6
279
m
P i t c h r a n g e (FRP)
E2
D3
I
I
C4 A#4 G#5 F#6 I
I
I
I
I
F N , n = 30
;,n=7 i
i
10 n=3
i
15 i
MN, n = 7
a
20 m
25
I
I
I
I
-20 -10 0 +10 +20 S t r a i n r a n g e (SR)
I
%
30
i
i
I
I
-21 -10 0 +10 +20 S t r a i n r a n g e (SR)
I
%
FIG. 3. Strain range (SR, gray areas) and the frequency range of phonation (FRP, horizontal bars) in female and male singers and nonsingers (FS, MS, FN, MN; Subset 1 in female nonsingers).
cal ranges, but only the range that was sung during radiography. From these values, average SR has been calculated for female and male singers and nonsingers. Typical strain values are below 20%. The dots in Figure 4 show the strain percentages calculated from measurements taken from radiographs; each x-ray is represented by one dot. The results are shown for female and male singers and nonsingers at all measured pitches. Strain percentages have been computed with the reference strain at D#4. The panels show the data points and average curves, calculated in pitch groups of 4 semitones. Linear regression lines describing the curves are steepest in female nonsingers (.64) and most level in male singers (.35). In male nonsingers the line is steeper than in female singers (.60 vs .50). To illustrate the relationship of curves describing strain percentage across pitch and the SSI, Figure 5 reproduces the curves for the female singers (n = 7). SSI values reflect the steepness of the strain-pitch curve.
On the whole, the curves are monotonic. At high pitches, the curves often level out. This is seen more clearly in Fig. 6, which gives the average strain percentage across pitch for each group. Figure 6 presents the average strain curves for female nonsingers and singers as well as male singers and nonsingers superimposed with the strain value at D4¢4 as the reference. The curves for males appear almost linear, even at the highest pitches, whereas the curve for female singers (and to some extent female nonsingers) resemble typical nonlinear stress-strain curves (1,36). At low pitches, women show a steeper increase in strain than men, whereas at midpitches the strain curves are practically identical for female and male subjects, which partly depends on the location of the reference strain. In high pitches, female subjects reach a higher strain percentage than male subjects. In all, female subjects have a wider range of strain than male subjects (about 20% vs about 15%). Journal of Voice, Vol. 12, No. 3, 1998
280
AATTO SONNINEN AND P E R T H HURME
M a l e s i n g e r s (n = 3) 15
,u
10
i
5
7 - - - -
M a l e n o n s i n g e r s (n = 7) 151
i
I
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F e m a l e n o n s i n g e r s (n = 50)
F e m a l e s i n g e r s (n = 7)
5
i ,:
C6
C7
.._. C2
Z_~_ C3
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.. s 5 1 . 7 ; . C5
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FIG. 4. The strain percentages for each female and male nonsinger and singer at all measured pitches.
Strain % 10
MS
..................
5
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0 F e m a l e s i n g e r s (n = 7) 15
•-"
.
.
.
.
.
.
.
.
.
.
.
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.
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.
-5
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MH .43
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/-v
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. HN .74
FIG. 5. The original vocal fold strain curves in female singers, with the SSI of each singer.
Journal of Voice, Vol. 12, No. 3, 1998
-15 -20
,
+
b
L
i
,
C2
C3
C4
C5
C6
C7
FIG. 6. Averaged frequency-strain curves for male nonsingers (MN), male singers (MS), female nonsingers (FN) and female singers (FS), adopted from Fig. 4. The curves have been superimposed with D#4 as the reference.
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
We present results below on the relation of the SSI and gender, age, voice training, and severing pretracheal muscles during thyroidectomy. Results pertaining to the measurement principle will also be presented.
Gender and training The measurements permit the comparison of female and male singers and nonsingers. The SSI (Fig. 4) is higher in nonsingers than singers: .58 in male singers, .63 in male nonsingers, .56 in female singers, and .72 in female nonsingers. However, the differences between the groups are not statistically significant. Figure 7 describes the frequency distribution of semitone strain indices calculated for female and male singers and nonsingers and in comparison for the Hollien and Moore (5) data. SSIs have been assigned to 20 categories from .25 to 2.15 at intervals of. 1. The columns indicate the number of subjects at each SSI. SSIs calculated from photographic data are higher (1.05-2.25) than from radiographic data (.25-1.55). In our data, males do not have SSIs higher than .95, whereas females show SSIs up to 1.45. Singers do not have SSIs higher than .85, whereas nonsingers show variation from .25 to 1.45. In sum, nonsingers used more strain (elongation) per one
281
semitone than singers and females used more strain (elongation) per one semitone than males. A more detailed analysis of one singer (EE Table 1), who sang a wide pitch range (each semitone up to G#6), allows the separate examination of two portions of the pitch range. In the lower portion ( - A # 4 ) the semitone strain index (based on the measurements of the T - A distance) is .81, but in the higher portion ( B 4 - ) the semitone strain is .29. The difference is statistically highly significant (p<.0001). Thus, as high pitch generally requires more stiffness (e.g., in EMG studies high pitches have been shown to be accompanied by high activity in the CT muscle), high SSI values may indicate low stiffness and low SSI values may indicate high stiffness in the vocal folds. This result is supported by stress-strain experiments (35,36). However, the activity of the TA muscle makes the relationship between stiffness and pitch more complicated, as discussed below.
Age hows the strain range in two groups of female nonsingers (Subset 1 in Table 1): the older subjects (cases 1-15; average age 51 years) and the younger subjects (cases 16-30; average age 30 years). The average
Subjects 14 12 10 8 6 4 2 0 tr~ ¢-,I
113
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o
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FIG. 7. The frequency distribution of semitone strain indices calculated for female and male singers and nonsingers (FS, MS, FN, MN) and for the Hollien and Moore data (H-M) (5). Journal of Voice, Vol. 12, No. 3, 1998
282
AATTO SONNINEN AND PERTTI HURME
FRP was significantly narrower in the older group (16 semitones) than in the younger group (21 semitones; p<.0057). The strain curve as described by linear regression is less steep (.44) in the older group than in the younger group (.77). The younger subjects show especially low strain values at lowest pitches (which the older subjects could not sing). , Figure 9 describes the frequency distribution of semitone strain indices calculated for the older and younger subjects. The SSI is significantly lower in the older group (.57) than in the younger group (.96; p< .0009). The simple linear correlation between SSI and age is significant (p<.0011). Other correlations (e.g., between age and highest note produced or strain percentage, or between strain and highest note produced or frequency range of phonation), were not significant. It can be concluded that younger female nonsingers exhibited more strain (elongation of vocal folds) per one semitone than older nonsingers.
Thyroideetomy The effect of bilaterally severing pretracheal muscles is examined by means of the semitone strain index in 19 cases of female nonsingers before and after thyroidectomy (Figure 10, Subset 2 in Table I). The correlation between the difference between the highest musical tone in semitones (HMT) before and after the operation with difference between SSI before and after the operation is almost significant (p< .02). The preoperational average of SSI is .76 and the postoperational average is.64. Thus, strain per one semitone was slightly smaller after bilaterally severing pretracheal muscles. Described by linear regression, the strain curve is less steep (.48) after the operation than before (.66).
F e m a l e n o n s i n g e r s (n = 30) • O l d e r subjects
[] Y o u n g e r subjects
15, 10. 5 0
T
".
-5
.
-10 rJ3 -15 -20 -25 -30 D#3
D#4
A#5
FIG. 8. Averaged strain curves and standard deviations in two groups of female nonsingers (Subset I): the older subjects (cases 1-15) and the younger subjects (cases 16-30).
Subjects 5 4 3 2 1 0
[--] Y o u n g e r
tr3 o-4
m
~
m
~
SSI
FIG. 9. The frequency distribution of semitone strain indices calculated for the older and younger subjects (Subset 1, n = 30).
Subjects
Method of measurement Figure 11 shows the strain percentages in the female nonsingers, where both T-C and T - A measurements could be taken (n = 15, Subset 3 in Table 1). The SSI values calculated from both measurements are also shown. In general, the indexes from T - A measurements are larger than from T-C measurements: .95 vs..73. A comparison of vocal fold strain ranges shows that the values closer to the actual strain values (T-A, 16.4%) are about 30% larger than those indicated by the T-C measurements (12.7%). Journal ofVoice, Vol. 12, No. 3, 1998
0 . . . . . . .
m
tn
tn
:11: :11:11: : m
tn
u~
iiii.e
u~
,
m
,,
m
: :1-1: tn SSI
FIG. 10. The frequency distribution of semitone strain indices calculated for female nonsingers (Subset 2) before and after thyroidectomy.
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
F e m a l e n o n s i n g e r s (n = 15) --T-C
T-A
15 I(1
.~
o
._r'i,r Strp I
-20
I
I ~tave
-25
.47 1.06
.49 .75
.55 .45
.60 .72
.62 .97
.64 . 6 9 T - C .81 . 9 1 T - A
10
-I0 -20
-25
SSI
.69 .72 1.09 1.00
.83 .84 .86 .93 1.00 1.09T-C .50 1.06 1.04 1.48 1.40 1.18 T-A
FIG. 11. The strain curves in the female nonsingers in which both T - C and T - A measurements could be taken. The SSI calculated from both measurements are also shown.
DISCUSSION The SSI calculated from T - A measurements probably better reflects the "real" movements of vocal folds, but unfortunately, there is more risk for measurement errors as the calcification points in the arytenoids are not always as clearly visible as in the cricoid cartilage. Therefore, we have to content ourselves with T-C, even though T - A would have been a better measure. The ability of the subjects (especially nonsingers) to sing at various pitches varied greatly: some were able to sing at three pitches and some were able to sing at seven pitches. Such differences decrease the reliability of the SSI. When calculating the value of the SSI, the choice of the reference length of the vocal folds is crucial. Here, the length at D#4 in millimeters was used. First, SSI was calculated for each individual by dividing the SR by the FRP. Group averages were then calculated from the individual SSIs. Group averages can be different (and less sensitive to individual variation) if the group average of strain range is divided by the group average of FRP.
283
Changes in strain with pitch were generally monotonic. However, vocal folds were not always smoothly elongated; occasionally, rather abrupt length adjustments (including shortening) were observed. It is evident that the reliability of the results is affected by the number of measurements taken. The division of the pitch range into portions with their own SSI also increases the accuracy of SSI. The results presented above are based on the assumption that the use of the reference level (the individual distance of T-C in millimeters when singing D#4 in the present study) is a valid method. Other levels of reference have been proposed, e.g., minimum length, length during respiration, and length during transcutaneous electrical stimulation of the recurrent laryngeal nerve (13). Such measures are, in our opinion, not superior to the method employed in the present study. With the reference level at D#4, elongation variation was standardized in relation to the T - A or T-C distance. The laryngeal behavior of individuals was examined on this basis. Theoretically, it is possible for stress or strain to be chosen as an independent variable. If strain is the independent variable, we are in accord with the following statement by Titze ( 1 p 42): "for equal longitudinal strain [italics ours] applied to the vocal folds, the greatest stress is developed in the epithelium, then in the ligament, and then in the thyroarytenoid muscle" The differences between the curves are due to differences in the extensibility of the layers. From the point of view of biomechanics and physiology, however, strain and pitch are dependent and stress (equaling external forces stretching the vocal folds) is always independent. There are anatomically and physiologically differing layers in the vocal folds (45). When a certain amount of external longitudinal stress (force) is applied to the epithelium or ligament (cover), the strain is relatively low compared to the strain of the muscle for the same amount of passive stress. Such is the case when the muscle is passive; if the body is activated, the situation can be the opposite: The strain of the body is less than the strain of the cover (36). According to Hirano (36), external stretching forces increase stress both in the cover and body, and internal contraction (in TA) increases stress in the body and decreases stress in cover layer. Consequently, the thyroarytenoid muscle regulates whether Journal of Voice, 'CoL 12, No. 3, 1998
284
AATTO SONNINEN AND PERTTI HURME
the body or the cover has greater stress (with constant external stress). This is in line with the hypothesis that the balancing (relative stiffening) of the body of the vocal fold with respect to the cover, and vice versa, is a major factor in pitch and register control in the voice (1,46). Therefore, a low SSI value does not always indicate greater stiffness than a high SSI value. Even if two individuals have the same SSI value, "they can differ in the stiffness of their vocal folds. When investigating vocal folds in living human beings, both strain and pitch are also determined by the stress of laryngeal muscles. The strain of the vocal folds can be relatively easily measured (if the ossification centers are visible in radiography). On the other hand, it is extremely difficult or even impossible at the present time to directly measure stress in a living human being (47). As stress values are not available. a range of pitch variation replaces stress and strain is examined at various pitches. Is the SSI useful? The curves describing strain and vocal pitch are nonlinear and resemble stress-strain curves (Fig. 4). In singing, the SSI is smaller in high pitch than in low pitch, probably indicating that stress (and possibly stiffness) has a high level in high vocal pitch and a low level in low pitch. Male subjects and singers have a lower semitone strain index (possibly indicating more stiffness) and female subjects and nonsingers have a higher index (possibly indicating less stiffness). The interpretation presented above is that low SSI indicates high inner stress and high SSI indicates low inner stress. This view receives tentative support from our observations; however, the contribution of the activity of the TA muscle complicates the relationship. Higher age is associated with lower semitone strain. In older individuals the connective tissue of the vocal folds can become stiffer ("fibrosis" of connective tissue, 48) and the stretching stress of external muscles weaker. In Fig. 8 the basic difference between the subjects can be seen only for the lowest pitch group, which is missing for the older subjects. The higher SSI of the younger subjects may thus be based on the way the semitone strain was calculated. Or could it be possible that stiffer vocal folds make it more difficult for the older subjects to sing the lowest tones? Titze (49) suggests that higher pitch in females is due to more stiffness and less elongation than in males. However, Fig. 6 shows that SSI is smaller and Journal of Voice, Vol. 12, No. 3, 1998
the stress-strain curve more linear for males than females, indicating that vocal fold tissue may be slightly stiffer in males than in females. This may be explained by the greater percentage of collagenous fibers in male than female vocal folds (48). However, it is clear that further comparative studies of the histological and microdynamic structure are needed. Is stiffness of tissue one of the factors accounting for differences between bass and tenor singers? Nonsingers use much strain to achieve their relatively narrow FRP, whereas singers use less strain and perhaps reduce the vibrating mass in accordance with the spring model: "to double the frequency of vibration, the m a s s . . , may be reduced to one-fourth its original size, or the spring constant . . . may be made four times larger" (50 p 20). The trained singer can relax the vocal muscle by means of "covering," whereby the cover of the vocal folds becomes stiffer. CONCLUSIONS i. The relationship between vocal fold strain and vocal pitch in singing a rising pitch series is described by the SSI which indicates standardized elongation of vocal folds by means of an average of vocal fold strain per one semitone. SSI is calculated by dividing the SR in percent by the FRP in semitones. 2. The relationship between vocal fold strain and vocal pitch is nonlinear and follows the stress-strain curve of organic tissue. 3. The SSI is influenced by structural and functional factors. Structural factors include: a) gender (SSI is higher in female than male subjects), b) age (SSI is higher in younger than older subjects), and c) organic insufficiency of strap muscles (SSI is lower after thyroidectomy than before the operation). The observed differences (which may indicate differences in stiffness) may be explained by the greater percentage of collagenous fibers and other connective tissue in males and in older subjects than in females and younger subjects. Functional factors include: (a) pitch placement (at lower pitches the SSI is higher than at higher pitches) and (b) vocal training (SSI is higher in nonsingers than singers). 4. Low SSI generally indicates much stiffness and high SSI indicates little stiffness in the vocal folds. However, even in cases where SSI is similar, there can be large differences in effective stiffness. Such differ-
VOCAL FOLD STRAIN AND VOCAL PITCH IN SINGING
ences may be due to variation in the structure of vocal fold tissue and to variation in the activity of the TA muscle. Measurements of a female singer singing a rising pitch series in semitone steps (to be reported by the present authors in a forthcoming publication) show that even when SSI remains about constant, greater effective stiffness in the vocal folds is manifested by typical changes in external laryngeal distances. 5. The SSI is a delicate measure. Because they are located between the thyroid cartilage and the arytenoid cartilages, the vocal folds cannot be directly measured in living human beings either by photography or by radiography. Sources of error in photography include the pulling of the tongue, the insertion of a mirror in the oropharynx, projection errors, and possibly the contraction of the laryngeal aditus (especially in higher pitches). It is also difficult to determine the exact point of measurement in the mucosa when using photographic methods. However, radiographic measurements also have problems. The risk of overexposure to radiation limits the use of the method on healthy subjects. The doses used in this study (where the material was collected 40 years ago) were low, with 100 exposures on the neck area corresponding to one exposure habitually used on the pelvic area. Radiographic methods are also hampered by the difficulty of selecting suitable subjects, as the ossification points are clearly visible in only about half of them. The radiographic measurements reported in this study are from the T-C distances. The results would be different if it had been possible to take T-A measurements, which better reflect the length of the vocal folds for all subjects. 6. Further studies exploring the factors that affect the SSI are needed to standardize the measurement procedure and to evaluate the significance of SSI.
Acknowledgments: We wish to thank Dr. Ronald Baken and three anonymous reviewers for their critical and constructive comments on an earlier version of this article. We are also grateful to Drs. Johan Sundberg, Erkki Vilkman, Anne-Maria Laukkanen, and Paavo Malinen for fruitful discussions.
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Journal of Voice, Vol. 12, No. 3, 1998
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