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Inspiratory Vocal Fry: Anatomical and Physiological Aspects, Application in Speech Therapy, Vocal Pedagogy and Singing. A Pilot study
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Inspiratory Vocal Fry: Anatomical and Physiological Aspects, Application in Speech Therapy, Vocal Pedagogy and Singing. A Pilot study *Nico P. Paolillo, †Luca Carrozza, *,‡Maurizio Osio, †Elisabetta Rosa, and †Matteo Scalabrin, *yzMilan, Italy Summary: Objective. Inspiratory Vocal Fry (IVF) is the voice production during inspiration of a sound with vocal fry perceptual characteristics. The existing scientific literature shows a lack of studies on it. The aim of the study is to highlight anatomical and physiological characteristics of IVF, to assess its effects on spoken and singing voice, to confirm the potential usefulness in speech therapy and vocal pedagogy. Methods. Thirty-two healthy subjects (17 male and 15 female) underwent videolaryngostroboscopy to assess the degree of false vocal folds adduction, pharyngeal wall contraction, and degree of vocal folds stretching in different types of phonation: expiratory and inspiratory phonation, Expiratory Vocal Fry (EVF) and IVF. All these parameters were evaluated by a group of three speech therapists and one phoniatrician not belonging to the research group. In addition, for each subject an electroglottography was performed for all the types of phonation previously mentioned, highlighting Contact Quotient (CQ) and Closing/Closed Quotient (CCQ). Three subjects underwent electromyography for a preliminary study of the muscle activation in IVF. Results. False vocal folds adduction (P value = 0.000005) and pharyngeal wall contraction (P value = 0.001155) were significantly reduced in IVF compared to EVF; on the contrary, vocal folds stretching was significantly higher in IVF (P value = 0.000031). Electroglottographic CQ was significantly higher in IVF compared to EVF (P value = 0.019592) and the other types of phonation. Similar results were obtained considering CCQ, as IVF values for this parameter was significantly higher compared to EVF (P value = 0.013062) and expiratory phonation (P value = 0.001324). As regards electromyography, medial thyroarytenoid (TA) motor units were more recruited in IVF, while lateral TA motor units were more recruited in EVF. According to our results, IVF is characterized by higher elastic tension due to a reduced hypertonic contraction of TA muscle and a higher contraction of cricothyroid muscle. Electroglottographic results showed a wider vibratory cycle with an improved massaging effect on vocal folds mucosa. electromyography preliminary analysis confirmed our findings. Conclusion. IVF could be an excellent and useful exercise to reduce muscular hypertonic tension and to facilitate mucosal elasticity. It could be potentially applied in speech therapy approach to dysfunctional and organic dysphonias, post-surgical treatment, in pedagogy and practice of artistic voice. Key Words: Inspiratory vocal fry−Electroglottography−Electromyography−Mucosal massage.
INTRODUCTION Inspiratory Vocal Fry (IVF) is the voice production during inspiration of a sound with vocal fry perceptual characteristics. The existing scientific literature shows a lack of studies on it. On the contrary, some authors analyzed anatomical and physiological features and functional effects on voice of Expiratory Vocal Fry (EVF) and Inspiratory Phonation (IP). Traditionally, EVF has been classified as a clinical syndrome associated with an atypical laryngeal emission.1 Moore and von Leden2 were probably the first researchers to detect the unusual vibratory pattern of vocal fry, which they termed dicrotic dysphonia,3 since they found a dicrotic vibratory pattern. A more detailed study on EVF was undertaken by Hollien1 who wrote that while the excessive use of fry could be diagnosed as a voice disorder, this Accepted for publication October 4, 2019. From the *University of Milan, Italy; yFreelancer, Milan; and the zDepartment of Neurology, Ospedale Sacco of Milan. Address correspondence and reprint requests to Nico Paolo Paolillo, ENT Department, Universit a degli Studi di Milano, viale Trieste 7, 20060 CASSINA DE' PECCHI, Milano, Italy. E-mail: [email protected] Journal of Voice, Vol. &&, No. &&, pp. &&−&& 0892-1997 © 2019 The Voice Foundation. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jvoice.2019.10.004
quality is too often heard in normal voices to be exclusively a disorder. Thus, he postulated that EVF is best described as a phonation register occurring at frequencies below those of the modal register. Nevertheless, it is important to note that the expression EVF mainly refers to the perception of the glottal vibration pulses during the exhaling voice emission. As for perceptual properties, EVF has been compared to the sound of a “motor boat,” to the “popping of corn”4 and to “food frying,”5 from which the expression “vocal fry” derives. Its main characteristic is a compact laryngeal structure with thick and short vocal folds because of the thyroarytenoid muscle shortening.6 The thickening of the vocal folds in combination with decreased vocal ligament stiffness during vocal fry may be the main causal factors to the reduced rate of vocal fold vibration, which therefore alter the characteristics of the vibratory cycle.4 Results from aerodynamic evaluations vary considerably. While most authors agree that EVF is featured by a reduced airstream,4,6,7 there are divergent findings regarding the subglottic pressure values, even though recent studies suggest that in EVF production it is possible to observe an increased subglottic pressure.6
ARTICLE IN PRESS 2 As for physiological properties, Whitehead et al8 using high-speed laryngeal photography found out that EVF vocal folds vibratory patterns can be associated with single, double, or triple opening and closing gestures. Subsequently, electroglottography (EGG) gave further information about vocal fry. Childers and Lee9 underlined that EVF is characterized by a glottal area function that has short pulses followed by a long closed glottal interval. Chen et al3 tried to extend the work of previous investigations by providing quantitative information concerning the glottal cycle symmetry in women and men during modal and vocal fry phonation. In their research both male and female speakers showed a significant increased Speed Quotient (SQ) in vocal fry phonation, suggesting that during the glottal cycle the vocal folds need a longer time to disconnect from each other compared to modal phonation. Higher values of Contact Quotient (CQ) were also found in vocal fry phonation compared to modal phonation for both males and females.10 Few authors investigated EVF effects on voice disorders and existing literature shows reduced and conflicting results on it as a facilitating technique. It's utility has been suggested in hyperkinetic dysphonias,6,11 in the improvement of the pneumophonic coordination, in the management of subglottic pressure,12 in the reduction of hypernasality and improvement of the velopharyngeal sphincter closure,13 in the correction of an overly breathy voice,14 and, especially in the past, in cases of organic lesions such as nodules, polyps, cysts, edema.6 Nevertheless, recent studies have hypothesized that EVF might be more efficient in glottal hypofunction rather than hyperfunction since it is produced with tightly adducted vocal folds.15 As for vocal pedagogy too, researchers have various opinions on the matter. Some authors suggest that EVF is a healthy production that can be applied to artistic singing16 and that it is a useful technique to extend the low range of baritones and basses17; others make no mention of it or are very open in its rejection as a phonatory mode like Cornelius Reid.18 Increasingly, this type of phonation is associated with modal register production in order to take advantage of the differences in vocal fold tension across different speaking registers helping the client to achieve increased control of vocal fold vibration and improved glottal closure.19 IP, also called reverse phonation, inhaling phonation or inverted phonation, is the voice production during air inflow into the lungs,20 which occurs naturally in different situations, including laughing, crying, and sighing.21 During IP there is an increase in subglottic pressure, favoring Bernoulli phenomenon,22 and in supraglottic pressure, determining ventricles relaxation and broadening of the laryngeal vestibule.20,23 Powers et al24 described it through the radiologic analysis as caused by the pressure created above the glottis through the turbulent air inflow, adducting the vocal folds. IP is characterized by a reduction of vocal folds contact because of the involvement of inspiratory muscles20,25 such as posterior cricoarytenoid and cricothyroid (CT) whose activity may antagonize the typically adductors.26
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FIGURE 1. An example of EVF voice production. Comparing this type of phonation to Expiratory Phonation (EP), it is possible to observe vocal folds lengthening related to CT contraction, quadrangular membrane elongation related to epiglottis anterior movement26 and reduction of false vocal folds contact.20 Orkiloff et al22 reported also a reduction in arytenoid compression. As for acoustic properties, during IP the fundamental frequency increases significantly in average of 74 Hz20,27 in comparison to EP. IP is used in vocal rehabilitation for those cases of psycogenic aphonya, puberphonias, mid-posterior triangular glottic slit, slit by vocal fold paresis, ventricular and aryepiglottic phonation, spasmodic dysphonia20 and stuttering.20,28 As for vocal pedagogy and singing, inhaling singing exists as a specific form of IP, which seems to require less effort in the high female register.29 Equal maximum phonation time (MPT) for inhaling singing and conventional singing in the lower register and a longer maximum phonation time in the higher register under the inhaling condition in comparison to conventional singing were observed by Vanhencke et al29 in opposition with previous studies on IP by Edgerton.30 It is important to state that there is no evidence of IVF in scientific and vocal pedagogy literature. Preliminary endoscopic evidences pointed out great differences in anatomical configuration and phonatory dynamic between EVF and IVF (Figures 1 and 2). In addition, positive effects of IVF were reported by professional voice users, who judged it very helpful to reduce muscle tension, to get vocal warm-up before vocalization, to achieve easily vocal cool-down
FIGURE 2. An example of IVF voice production.
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without losing vocal folds tone, and to avoid vocal fatigue during difficult performances. Moreover, good results in patients with voice disorders were obtained by speech therapists too after a first empirical application of this technique. Thus, the aim of this pilot study is—highlighting anatomical and physiological aspects of IVF, assessing its effects on spoken and singing voice, and evaluating its potential usefulness in speech therapy, vocal pedagogy and singing. MATERIAL AND METHODS Sample Thirty-two healthy subjects (17 males and 15 females) aged between 20 and 56 years without voice complaints nor vocal folds pathologies and able to sustain EP, IP, EVF, and IVF participated in the present study, which was conducted in a private medical office, prior signed consent. First, the 32 volunteers were asked to produce for few seconds (from 4 to 8 seconds) the four different types of phonation analyzed in the research. EP, IP, EVF, and IVF exact production was perceptually judged by the research team members. Nine subjects were not able to perform IVF at the first time. For all of them facilitating techniques were successfully applied to achieve the correct production. Thus, no one was excluded from this preliminary test. The facilitating techniques were starting the emission from the nose with closed lips and relaxed jaw, striving to produce the inspiratory sound quickly and strongly, protruding the tongue, reverse laugh, producing a very low note followed without interruption by an IP trying to maintain the same Fundamental Frequency (F0), and focusing on diaphragmatic activity.
Procedures The 32 volunteers underwent videolaryngostroboscopy to assess three parameters which were − false vocal folds adduction, pharyngeal wall contraction, and vocal folds stretching. The KAYPENTAX 9400 HD laryngeal strobe was used. Each subject was asked to sustain for few seconds (from 4 to 8 seconds) the vowel /i/ for EP, at a comfortable modal pitch and loudness, and EVF and a neutral sound for IVF; four examiners expert in voice (three speech and language pathologists and one phoniatrician) not belonging to the research group assigned to each parameter a score on a scale which went from 0, meaning none, to 5, the maximum. For each parameter, subject, and type of phonation mean scores were made. Two subjects were excluded from the analysis due to the impossibility of carrying out the examination because of pharyngeal reflexes. Subsequently, all the volunteers underwent EGG. The KAYPENTAX 6013 electroglottograph was used. They were asked to produce for few seconds (from 4 to 8 seconds) the vowel /a/ for EP, at a comfortable modal pitch and loudness, and EVF and a neutral sound for IP and IVF. The final data provided by the analysis software were the mean values in percent of CQ, which is a ratio that illustrates the duration of vocal folds contact during each vibratory cycle,
3 and Closing/Closed Quotient (CCQ), which is the ratio between the phase of approach and separation of the free edges of the vocal folds and the total contact time of the same ones. Four subjects were excluded because of registration artifacts that led to unrealistic measures. Finally, three subjects underwent electromyography (EMG) to assess the turns of median and lateral TA muscles producing for few seconds EVF and IVF. Turns can be defined as changes in signal direction at the peak of motor unit signal with each successive turn separated by greater than 100 mV to exclude low-amplitude peaks generated by noise and electrical interference. Turns analysis quantitatively measures the interference pattern, which describes motor unit recruitment.31 It was possible to carry out both registrations of the median and lateral TA muscles only for one subject due to the reduced compliance of the others.
Statistical analysis Considering that this project is a pilot study with a reduced sample, it was not recommended to perform a formal normality test, such as the Kolmogorov-Smirnov one, to verify the results distribution. Thus, for all the procedures hystograms highlighting the results distributions were created together with their qualitative interpretation. All the distributions seemed non-Gaussian; this fact was supported also by almost all the results of the Kolmogorov-Smirnov test, which was carried out just to confirm that the qualitative interpretation was correct, even if this procedure, as previously mentioned, was not recommended. Since we found out that almost all the distributions were non-Gaussian, for all the procedures the Wilcoxon Signed-Ranks test for matched pairs was performed to evaluate the significance of the obtained results comparing each type of phonation and establishing the significance level at P value lower than 0.05. As the verification of different hypothesis on the same data sample increases false positive error probability, the Bonferroni correction (BC) was performed. Nevertheless, since it is particularly conservative and since this is a pilot study aimed at proposing hypothesis rather than verifying demonstrations, it was not taken into account. RESULTS Videolaryngostroboscopy As for the videolaryngostroboscopy analysis, the three types of phonation (EP, EVF, and IVF) were compared to each other after calculating for each subject the average of the scores assigned by the four examiners. False vocal folds adduction was significantly reduced in IVF (Figure 1) compared to EVF (Figure 2) and in EP compared to EVF. No significant difference was found comparing IVF to EP (Table 1). Pharyngeal wall contraction was significantly reduced in IVF (Figure 1) compared to EVF (Figure 2), in EP compared to EVF and in EP compared to IVF, even though, considering the BC, no significant difference was found between IVF and EP (Table 2). Vocal folds stretching
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TABLE 1. False Vocal Folds Adduction: Significance of the Results P value IVF vs EVF 0.000005 EVF vs EP 0.000004 IVF vs EP 0.569494
Significance Yes Yes No
P value Significance (BC) (BC) 0.000015 0.000020 1.708482
Yes Yes No
TABLE 2. Pharyngeal Wall Contraction: Significance of the Results P value Significance IVF vs EVF 0.001155 EVF vs EP 0.000060 IVF vs EP 0.020795
Yes Yes Yes
P value Significance (BC) (BC) 0.003465 0.00018 0.062385
Yes Yes No
comparison was made between IVF (Figure 1) and EVF (Figure 2). This parameter was significantly higher in IVF compared to EVF (Table 3). Electroglottography Considering previous studies concerning EVF EGG characteristics compared to EP ones, the research team decided to take into account only comparisons between IVF and the other types of phonation. Electroglottographic CQs were significantly higher in IVF compared to EP, to IP and to EVF (Table 4). Similar results were obtained considering CCQ, as IVF values for this parameter were significantly higher compared to EVF and EP. No significant difference was found between IVF and IP (Table 5). Electromyography As previously mentioned, for the EMG analysis it was possible to carry out both registrations of the medial and lateral TABLE 3. Vocal Folds Stretching: Significance of the Results P value IVF vs EVF 0.000031
Significance Yes
P value Significance (BC) (BC) /
/
TABLE 4. CQ: Significance of the Results P value IVF vs EP 0.000321 IVF vs IP 0.000269 IVF vs EVF 0.019592
Significance Yes Yes Yes
TABLE 5. CCQ: Significance of the Results
P value Significance (BC) (BC) 0.001926 0.001614 0.117552
Yes Yes No
P value
Significance
IVF vs EP 0.001324 IVF vs IP 0.553812 IVF vs EVF 0.013062
Yes No Yes
P value Significance (BC) (BC) 0.007944 3.322872 0.078372
Yes No No
TABLE 6. EMG: Significance of the Results Lateral TA Subject P-value 1 2 3
0.032130 0.000655 /
Medial TA
Significance P value Yes Yes /
0.006910 / 0.073138
Significance Yes / No
TA muscles only for one subject due to the reduced compliance of the others. Thus, for the first subject both the muscles were analyzed, while for the second and the third subject only medial TA and lateral TA, respectively were considered. As for the results of the first subject, medial TA motor units were significantly more recruited in IVF compared to EVF, while lateral TA motor units were significantly more recruited in EVF compared to IVF. The third subject obtained similar results in the analysis of lateral TA muscle, which was significantly recruited more in EVF in comparison to IVF. No significant difference in the assessment of medial TA in the second subject was found, even though IVF turns were higher compared to EVF ones, as for the first subject (Table 6). DISCUSSION This first pilot study on IVF aims to carry out its anatomical and physiological features, to evaluate its effects on spoken and singing voice, to confirm its utility reported by professional voice users and the good results obtained after a first empirical application in patients with voice disorders. At the beginning of the project, the nomenclature matter was discussed. It is important to clarify that the research team decided to use the expression “Inspiratory Vocal Fry” for this new type of voice production exclusively referring to the perception of the glottal vibration pulses during the voice emission, as it happens with EVF, even though the effective anatomical and physiological characteristics of this type of phonation was unknown. As for videolaryngostroboscopy, false vocal folds adduction was significantly reduced in IVF compared to EVF, highlighting a balancing between adductor and abductor forces and a reduction of hyperkinetic attitude in IVF. These evidences were confirmed by the EMG results, which showed for the analyzed subjects a reduced activity in IVF
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of lateral TA, which directly influences false vocal folds movements. No significant difference was found between IVF and EP at a comfortable pitch and loudness, supporting the hypothesis that both these types of phonation are not characterized by a hyperkinetic attitude. Pharyngeal wall contraction values were significantly lower in IVF compared to EVF, meaning that configurational variations exist not only at laryngeal level, but also at pharyngeal level and confirming a nonhyperkinetic attitude in IVF. As for the comparison between IVF and EP, a significantly higher pharyngeal wall contraction in IVF was found, even though in this case the BC showed a nonsignificant difference. It can be hypothesized that in IVF the pharyngeal wall muscles maintain a tonic contraction without reaching the hyperkinetic attitude, which is typical of EVF. Vocal folds' stretching is significantly higher in IVF compared to EVF, because of the contraction of CT muscles which increase vocal folds stretching, elastic and nonhypertonic tension. For this analysis, EP was not compared to IVF and EVF because in this type of phonation, at a comfortable pitch and loudness, it is already known that there is not an increased activity of CT. Electroglottographic CQs were significantly higher in IVF compared to EVF and the other types of phonation highlighting a nontight adduction with elastic tension of the vocal muscle and, therefore, a reduced transglottic pressure gradient in IVF. Similar results were obtained considering CCQ, as IVF values for this parameter were significantly higher compared to EVF and EP, meaning that IVF is characterized by a more prolonged time of approach and separation between the free edges of the vocal folds and therefore a greater “massaging effect.” As regard EMG, medial TA motor units were more recruited in IVF, while lateral TA motor units were more recruited in EVF. According to these preliminary findings, it is possible to state that IVF is characterized by a clear phase difference in vibratory pattern between the mucosal layer, which freely vibrates, and the muscle-ligament one, which is static due to the elastic contraction of the medial TA. This anatomical configuration consequently allows a “massage” only for the mucosal layer. On the other hand, EVF is characterized by a low phase difference in vibratory pattern between muscle-ligament layer and mucosa, which simultaneously and compactly vibrate, due to medial TA relaxation. Nine subjects of the sample were not able to perform IVF at the first time. The following facilitating techniques, used empirically in everyday clinical practice, were successfully applied in order to achieve the correct production of IVF for all of them: starting the emission from the nose with closed lips and relaxed jaw, striving to produce the inspiratory sound quickly and strongly, protruding the tongue, reverse laugh, producing a very low note followed without interruption by an IP trying to maintain the same Fundamental Frequency (F0), and focusing on diaphragmatic activity. Considering the results of this study, similar properties between IVF and IP were found. As a matter of fact, as IP, IVF seems to be characterized by a synergy between
adductor and abductor muscles and a laryngeal lowering tendency. IVF can be described as a different vocal register in comparison to EVF, since it is associated with different laryngeal muscle activity, synergy, and anatomical configuration. Nevertheless, as previously mentioned, the expression “Inspiratory Vocal Fry” refers to the perception of the glottal vibration pulses during the voice emission. According to the results of this study, IVF can be hypothesized as a valid and safe technique since it improves glottic muscle elasticity and relaxation of supraglottic structures, reduces the hyperkinetic tendency, and allows an effective mucosal massage. Thus, in speech therapy it could be potentially useful in case of dysfunctional and organic dysphonias, postsurgical rehabilitation, and rehabilitation of the artistic voice, although further evidence is needed. For the same reasons, in vocal pedagogy and singing, it could be potentially suitable in vocal warm-up to facilitate the correct muscular and subglottic pressure balance, during the performance as a method to reduce muscular tension after fatiguing vocal tasks, in vocal cool-down after demanding performances, and to reduce frequent hyperfunctional behaviors typical of beginners. In this field, specific studies are desirable too. The limitations of the study are mostly related to the intrinsic properties of the pilot study. As regards the future perspectives, it could be useful to study what happens in case of vocal folds pathology and inflammation, the real effectiveness and applicability in the speech therapy of dysphonias and to improve the corpus of facilitating exercises. CONCLUSIONS The present study provides a preliminary insight on anatomical and physiological features of IVF, which is the voice production during inspiration of a sound with vocal fry perceptual characteristics. Considering IVF laryngeal muscle activity, synergy, and anatomical configuration highlighted in this study, it is possible to state that IVF is a different vocal register in comparison to EVF. The results of this project confirm that, as initially observed at a first empirical application on patients with voice disorders, IVF could be an excellent technique to reduce muscular hypertonic tension and to facilitate mucosal elasticity. It could be applied in speech therapy approach to dysfunctional and organic dysphonias, postsurgical treatment, in vocal pedagogy and practice of artistic voice. SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/10.1016/j. jvoice.2019.10.004. REFERENCES 1. Hollien H, Moore P, Wendhal R, et al. On the nature of vocal fry. J Speech Hear Res. 1966;9:245–247.
ARTICLE IN PRESS 6 2. Moore P, Von Leden H. Dynamic variations of the vibratory pattern in the normal larynx. Folia Phoniatr (Basel). 1958;10:205–238. 3. Chen Y, Robb MP, Gilbert HR. Electroglottographic evaluation of gender and vowel effects during modal and vocal fry phonation. J Speech Lang Hear Res. 2002;45:821–829. 4. Blomgren M, Chen Y, Ng ML, et al. Acoustic, aerodynamic, physiologic and perceptual properties of modal and vocal fry registers. J Acoust Soc Am. 1998;103:2649–2658. 5. Ishi CT, Sakakibara KI, Ishiguro H, et al. A method for automatic detection of vocal fry. IEEE Trans Audio Speech Lang Proc. 2008;16:47–56. 6. Cielo CA, Elias VS, Brum DM, et al. Thyroarytenoid muscle and vocal fry: a literature review. Rev Sociedade Bras Fonoaudiologia. 2011;16:362–369. 7. Murry T. Subglottal pressure and airflow measures during vocal fry phonation. J Speech Hear Res. 1971;14:544–551. 8. Whitehead R, Metz D, Whitehead G. Vibratory patterns of the vocal folds during pulse register phonation. J Acoust Soc Am. 1984;75:1293– 1297. 9. Childers D, Lee C. Vocal qualities factors: analysis, synthesis, and perception. J Acoust Soc Am. 1991;90. 23942410. 10. Paul N, Kumar S, Chatterjee I, et al. Electroglottographic parameterization of the effects of gender, vowel and phonatory registers on vocal fold vibratory patterns: an Indian perspective. Indian J Otolaryngol Head Neck Surg. 2011;63:27–31. 11. Boone DR, McFarlane SC, Von Berg SL, et al. The Voice and Voice Theraphy. Boston, Massachussetts: Allyn & Bacon; 2010. 12. Mazzocchi R, Panzanelli R, Brizi S, et al. L’utilita del vocal fry nell’educazione della voce parlata e cantata: nostra esperienza. Atti XXXVI Convegno nazionale SIFEL. Modena; 2002. 13. Elias VS, Cielo CA, Jotz G, et al. Effect of vocal fry on voice and on velopharyngeal sphincter. Int Arch Otorhinolaryngol. 2015;20:156– 162. 14. Vennard W. Singing: The Mechanism and the Technic. rev.ed. New York: Carl Fisher; 1967. 15. Meerschman I, D’haeseleer E, Catry T, et al. Effect of two isolated vocal facilitating techniques glottal fry and yawn-sigh on the phonation of female speech-language pathology students: a pilot study. J Commun Disord. 2017;66:40–50.
Journal of Voice, Vol. &&, No. &&, 2019 16. Nix J, Emerich K, Titze IR. Application of vocal fry to the training of singers. J Singing. 2005;62:53–59. 17. Stark J. Bel Canto: A History of Vocal Pedagogy. Toronto: University of Toronto Press; 1999. 18. Reid C. A Dictionary of Vocal Terminology: An Analysis. New York: Joseph Patelson; 1983. 19. Behrman A, Haskell J. Exercises for Voice Therapy. 3rd ed San Diego: Plural Publishing Inc.; 2019. 20. Finger LS, Cielo CA. Reverse phonation - physiologic and clinical aspects of this speech voice therapy modality. Braz J Otorhinolaryngol. 2007;73:271–277. 21. Timcke R, von Leden H, Moore P. Laryngeal vibrations: measurement of the glottal wave. Part II: physiologic variations. Am Med Assoc Arch Otolaryngol. 1959;69:438–444. 22. Orkiloff RF, Baken RJ, Kraus DH. Acoustic and physiologic characteristics of inspiratory phonation. J Acoust Soc Am. 1997;102:1838–1845. 23. Lehman MDQH. Reverse phonation: a new maneuver for examining the larynx. Radiology. 1965;84:215–222. 24. Powers WE, Holtz S, Ogura J. Contrast examination of the larynx and pharynx: inspiratory phonation. Am J Roentgenol. 1964;92:40–42. 25. Harrison GA, Troughear RH, Davis P, et al. Inspiratory speech as a management option for spastic dysphonia: case study. Ann Otol Rhinol Laryngol. 1992;101:375–382. 26. Kelly C, Fisher K. Stroboscopic and acoustic measures of inspiratory phonation. J Voice. 1999;13:389–402. 27. Roob MP, Chen Y, Gilbert HR, et al. Acoustic comparison of vowel articulation in normal and reverse phonation. J Speech Lang Hear Res. 2001;44:118–127. 28. Kenjo M. Treatment featuring direct speech therapy for a school age child with severe stuttering: a case report. Jap J Logop Phoniatr. 2005;46:21. 29. Vanhecke F, Moerman M, Desmet F, et al. Acoustical properties in inhaling singing: a case study. Phys Med. 2017;3:9–15. 30. Edgerton ME. The 21st Century Voice: Contemporary and Traditional Extra-normal Voice. 2 ed Lanham, Maryland: Rowman & Littlefield; 2004. 31. Smith LJ, Rosen CA, Niyonkuru C, et al. Quantitative electromyography improves prediction in vocal fold paralysis. Laryngoscope. 2012;122: 854859.
Inspiratory Vocal Fry: Anatomical and Physiological Aspects, Application in Speech Therapy, Vocal Pedagogy and Singing. A Pilot study *Nico P. Paolillo, †Luca Carrozza, *,‡Maurizio Osio, †Elisabetta Rosa, and †Matteo Scalabrin, *yzMilan, Italy Summary: Objective. Inspiratory Vocal Fry (IVF) is the voice production during inspiration of a sound with vocal fry perceptual characteristics. The existing scientific literature shows a lack of studies on it. The aim of the study is to highlight anatomical and physiological characteristics of IVF, to assess its effects on spoken and singing voice, to confirm the potential usefulness in speech therapy and vocal pedagogy. Methods. Thirty-two healthy subjects (17 male and 15 female) underwent videolaryngostroboscopy to assess the degree of false vocal folds adduction, pharyngeal wall contraction, and degree of vocal folds stretching in different types of phonation: expiratory and inspiratory phonation, Expiratory Vocal Fry (EVF) and IVF. All these parameters were evaluated by a group of three speech therapists and one phoniatrician not belonging to the research group. In addition, for each subject an electroglottography was performed for all the types of phonation previously mentioned, highlighting Contact Quotient (CQ) and Closing/Closed Quotient (CCQ). Three subjects underwent electromyography for a preliminary study of the muscle activation in IVF. Results. False vocal folds adduction (P value = 0.000005) and pharyngeal wall contraction (P value = 0.001155) were significantly reduced in IVF compared to EVF; on the contrary, vocal folds stretching was significantly higher in IVF (P value = 0.000031). Electroglottographic CQ was significantly higher in IVF compared to EVF (P value = 0.019592) and the other types of phonation. Similar results were obtained considering CCQ, as IVF values for this parameter was significantly higher compared to EVF (P value = 0.013062) and expiratory phonation (P value = 0.001324). As regards electromyography, medial thyroarytenoid (TA) motor units were more recruited in IVF, while lateral TA motor units were more recruited in EVF. According to our results, IVF is characterized by higher elastic tension due to a reduced hypertonic contraction of TA muscle and a higher contraction of cricothyroid muscle. Electroglottographic results showed a wider vibratory cycle with an improved massaging effect on vocal folds mucosa. electromyography preliminary analysis confirmed our findings. Conclusion. IVF could be an excellent and useful exercise to reduce muscular hypertonic tension and to facilitate mucosal elasticity. It could be potentially applied in speech therapy approach to dysfunctional and organic dysphonias, post-surgical treatment, in pedagogy and practice of artistic voice. Key Words: Inspiratory vocal fry−Electroglottography−Electromyography−Mucosal massage.
INTRODUCTION Inspiratory Vocal Fry (IVF) is the voice production during inspiration of a sound with vocal fry perceptual characteristics. The existing scientific literature shows a lack of studies on it. On the contrary, some authors analyzed anatomical and physiological features and functional effects on voice of Expiratory Vocal Fry (EVF) and Inspiratory Phonation (IP). Traditionally, EVF has been classified as a clinical syndrome associated with an atypical laryngeal emission.1 Moore and von Leden2 were probably the first researchers to detect the unusual vibratory pattern of vocal fry, which they termed dicrotic dysphonia,3 since they found a dicrotic vibratory pattern. A more detailed study on EVF was undertaken by Hollien1 who wrote that while the excessive use of fry could be diagnosed as a voice disorder, this Accepted for publication October 4, 2019. From the *University of Milan, Italy; yFreelancer, Milan; and the zDepartment of Neurology, Ospedale Sacco of Milan. Address correspondence and reprint requests to Nico Paolo Paolillo, ENT Department, Universit a degli Studi di Milano, viale Trieste 7, 20060 CASSINA DE' PECCHI, Milano, Italy. E-mail: [email protected] Journal of Voice, Vol. &&, No. &&, pp. &&−&& 0892-1997 © 2019 The Voice Foundation. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jvoice.2019.10.004
quality is too often heard in normal voices to be exclusively a disorder. Thus, he postulated that EVF is best described as a phonation register occurring at frequencies below those of the modal register. Nevertheless, it is important to note that the expression EVF mainly refers to the perception of the glottal vibration pulses during the exhaling voice emission. As for perceptual properties, EVF has been compared to the sound of a “motor boat,” to the “popping of corn”4 and to “food frying,”5 from which the expression “vocal fry” derives. Its main characteristic is a compact laryngeal structure with thick and short vocal folds because of the thyroarytenoid muscle shortening.6 The thickening of the vocal folds in combination with decreased vocal ligament stiffness during vocal fry may be the main causal factors to the reduced rate of vocal fold vibration, which therefore alter the characteristics of the vibratory cycle.4 Results from aerodynamic evaluations vary considerably. While most authors agree that EVF is featured by a reduced airstream,4,6,7 there are divergent findings regarding the subglottic pressure values, even though recent studies suggest that in EVF production it is possible to observe an increased subglottic pressure.6
ARTICLE IN PRESS 2 As for physiological properties, Whitehead et al8 using high-speed laryngeal photography found out that EVF vocal folds vibratory patterns can be associated with single, double, or triple opening and closing gestures. Subsequently, electroglottography (EGG) gave further information about vocal fry. Childers and Lee9 underlined that EVF is characterized by a glottal area function that has short pulses followed by a long closed glottal interval. Chen et al3 tried to extend the work of previous investigations by providing quantitative information concerning the glottal cycle symmetry in women and men during modal and vocal fry phonation. In their research both male and female speakers showed a significant increased Speed Quotient (SQ) in vocal fry phonation, suggesting that during the glottal cycle the vocal folds need a longer time to disconnect from each other compared to modal phonation. Higher values of Contact Quotient (CQ) were also found in vocal fry phonation compared to modal phonation for both males and females.10 Few authors investigated EVF effects on voice disorders and existing literature shows reduced and conflicting results on it as a facilitating technique. It's utility has been suggested in hyperkinetic dysphonias,6,11 in the improvement of the pneumophonic coordination, in the management of subglottic pressure,12 in the reduction of hypernasality and improvement of the velopharyngeal sphincter closure,13 in the correction of an overly breathy voice,14 and, especially in the past, in cases of organic lesions such as nodules, polyps, cysts, edema.6 Nevertheless, recent studies have hypothesized that EVF might be more efficient in glottal hypofunction rather than hyperfunction since it is produced with tightly adducted vocal folds.15 As for vocal pedagogy too, researchers have various opinions on the matter. Some authors suggest that EVF is a healthy production that can be applied to artistic singing16 and that it is a useful technique to extend the low range of baritones and basses17; others make no mention of it or are very open in its rejection as a phonatory mode like Cornelius Reid.18 Increasingly, this type of phonation is associated with modal register production in order to take advantage of the differences in vocal fold tension across different speaking registers helping the client to achieve increased control of vocal fold vibration and improved glottal closure.19 IP, also called reverse phonation, inhaling phonation or inverted phonation, is the voice production during air inflow into the lungs,20 which occurs naturally in different situations, including laughing, crying, and sighing.21 During IP there is an increase in subglottic pressure, favoring Bernoulli phenomenon,22 and in supraglottic pressure, determining ventricles relaxation and broadening of the laryngeal vestibule.20,23 Powers et al24 described it through the radiologic analysis as caused by the pressure created above the glottis through the turbulent air inflow, adducting the vocal folds. IP is characterized by a reduction of vocal folds contact because of the involvement of inspiratory muscles20,25 such as posterior cricoarytenoid and cricothyroid (CT) whose activity may antagonize the typically adductors.26
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FIGURE 1. An example of EVF voice production. Comparing this type of phonation to Expiratory Phonation (EP), it is possible to observe vocal folds lengthening related to CT contraction, quadrangular membrane elongation related to epiglottis anterior movement26 and reduction of false vocal folds contact.20 Orkiloff et al22 reported also a reduction in arytenoid compression. As for acoustic properties, during IP the fundamental frequency increases significantly in average of 74 Hz20,27 in comparison to EP. IP is used in vocal rehabilitation for those cases of psycogenic aphonya, puberphonias, mid-posterior triangular glottic slit, slit by vocal fold paresis, ventricular and aryepiglottic phonation, spasmodic dysphonia20 and stuttering.20,28 As for vocal pedagogy and singing, inhaling singing exists as a specific form of IP, which seems to require less effort in the high female register.29 Equal maximum phonation time (MPT) for inhaling singing and conventional singing in the lower register and a longer maximum phonation time in the higher register under the inhaling condition in comparison to conventional singing were observed by Vanhencke et al29 in opposition with previous studies on IP by Edgerton.30 It is important to state that there is no evidence of IVF in scientific and vocal pedagogy literature. Preliminary endoscopic evidences pointed out great differences in anatomical configuration and phonatory dynamic between EVF and IVF (Figures 1 and 2). In addition, positive effects of IVF were reported by professional voice users, who judged it very helpful to reduce muscle tension, to get vocal warm-up before vocalization, to achieve easily vocal cool-down
FIGURE 2. An example of IVF voice production.
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without losing vocal folds tone, and to avoid vocal fatigue during difficult performances. Moreover, good results in patients with voice disorders were obtained by speech therapists too after a first empirical application of this technique. Thus, the aim of this pilot study is—highlighting anatomical and physiological aspects of IVF, assessing its effects on spoken and singing voice, and evaluating its potential usefulness in speech therapy, vocal pedagogy and singing. MATERIAL AND METHODS Sample Thirty-two healthy subjects (17 males and 15 females) aged between 20 and 56 years without voice complaints nor vocal folds pathologies and able to sustain EP, IP, EVF, and IVF participated in the present study, which was conducted in a private medical office, prior signed consent. First, the 32 volunteers were asked to produce for few seconds (from 4 to 8 seconds) the four different types of phonation analyzed in the research. EP, IP, EVF, and IVF exact production was perceptually judged by the research team members. Nine subjects were not able to perform IVF at the first time. For all of them facilitating techniques were successfully applied to achieve the correct production. Thus, no one was excluded from this preliminary test. The facilitating techniques were starting the emission from the nose with closed lips and relaxed jaw, striving to produce the inspiratory sound quickly and strongly, protruding the tongue, reverse laugh, producing a very low note followed without interruption by an IP trying to maintain the same Fundamental Frequency (F0), and focusing on diaphragmatic activity.
Procedures The 32 volunteers underwent videolaryngostroboscopy to assess three parameters which were − false vocal folds adduction, pharyngeal wall contraction, and vocal folds stretching. The KAYPENTAX 9400 HD laryngeal strobe was used. Each subject was asked to sustain for few seconds (from 4 to 8 seconds) the vowel /i/ for EP, at a comfortable modal pitch and loudness, and EVF and a neutral sound for IVF; four examiners expert in voice (three speech and language pathologists and one phoniatrician) not belonging to the research group assigned to each parameter a score on a scale which went from 0, meaning none, to 5, the maximum. For each parameter, subject, and type of phonation mean scores were made. Two subjects were excluded from the analysis due to the impossibility of carrying out the examination because of pharyngeal reflexes. Subsequently, all the volunteers underwent EGG. The KAYPENTAX 6013 electroglottograph was used. They were asked to produce for few seconds (from 4 to 8 seconds) the vowel /a/ for EP, at a comfortable modal pitch and loudness, and EVF and a neutral sound for IP and IVF. The final data provided by the analysis software were the mean values in percent of CQ, which is a ratio that illustrates the duration of vocal folds contact during each vibratory cycle,
3 and Closing/Closed Quotient (CCQ), which is the ratio between the phase of approach and separation of the free edges of the vocal folds and the total contact time of the same ones. Four subjects were excluded because of registration artifacts that led to unrealistic measures. Finally, three subjects underwent electromyography (EMG) to assess the turns of median and lateral TA muscles producing for few seconds EVF and IVF. Turns can be defined as changes in signal direction at the peak of motor unit signal with each successive turn separated by greater than 100 mV to exclude low-amplitude peaks generated by noise and electrical interference. Turns analysis quantitatively measures the interference pattern, which describes motor unit recruitment.31 It was possible to carry out both registrations of the median and lateral TA muscles only for one subject due to the reduced compliance of the others.
Statistical analysis Considering that this project is a pilot study with a reduced sample, it was not recommended to perform a formal normality test, such as the Kolmogorov-Smirnov one, to verify the results distribution. Thus, for all the procedures hystograms highlighting the results distributions were created together with their qualitative interpretation. All the distributions seemed non-Gaussian; this fact was supported also by almost all the results of the Kolmogorov-Smirnov test, which was carried out just to confirm that the qualitative interpretation was correct, even if this procedure, as previously mentioned, was not recommended. Since we found out that almost all the distributions were non-Gaussian, for all the procedures the Wilcoxon Signed-Ranks test for matched pairs was performed to evaluate the significance of the obtained results comparing each type of phonation and establishing the significance level at P value lower than 0.05. As the verification of different hypothesis on the same data sample increases false positive error probability, the Bonferroni correction (BC) was performed. Nevertheless, since it is particularly conservative and since this is a pilot study aimed at proposing hypothesis rather than verifying demonstrations, it was not taken into account. RESULTS Videolaryngostroboscopy As for the videolaryngostroboscopy analysis, the three types of phonation (EP, EVF, and IVF) were compared to each other after calculating for each subject the average of the scores assigned by the four examiners. False vocal folds adduction was significantly reduced in IVF (Figure 1) compared to EVF (Figure 2) and in EP compared to EVF. No significant difference was found comparing IVF to EP (Table 1). Pharyngeal wall contraction was significantly reduced in IVF (Figure 1) compared to EVF (Figure 2), in EP compared to EVF and in EP compared to IVF, even though, considering the BC, no significant difference was found between IVF and EP (Table 2). Vocal folds stretching
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TABLE 1. False Vocal Folds Adduction: Significance of the Results P value IVF vs EVF 0.000005 EVF vs EP 0.000004 IVF vs EP 0.569494
Significance Yes Yes No
P value Significance (BC) (BC) 0.000015 0.000020 1.708482
Yes Yes No
TABLE 2. Pharyngeal Wall Contraction: Significance of the Results P value Significance IVF vs EVF 0.001155 EVF vs EP 0.000060 IVF vs EP 0.020795
Yes Yes Yes
P value Significance (BC) (BC) 0.003465 0.00018 0.062385
Yes Yes No
comparison was made between IVF (Figure 1) and EVF (Figure 2). This parameter was significantly higher in IVF compared to EVF (Table 3). Electroglottography Considering previous studies concerning EVF EGG characteristics compared to EP ones, the research team decided to take into account only comparisons between IVF and the other types of phonation. Electroglottographic CQs were significantly higher in IVF compared to EP, to IP and to EVF (Table 4). Similar results were obtained considering CCQ, as IVF values for this parameter were significantly higher compared to EVF and EP. No significant difference was found between IVF and IP (Table 5). Electromyography As previously mentioned, for the EMG analysis it was possible to carry out both registrations of the medial and lateral TABLE 3. Vocal Folds Stretching: Significance of the Results P value IVF vs EVF 0.000031
Significance Yes
P value Significance (BC) (BC) /
/
TABLE 4. CQ: Significance of the Results P value IVF vs EP 0.000321 IVF vs IP 0.000269 IVF vs EVF 0.019592
Significance Yes Yes Yes
TABLE 5. CCQ: Significance of the Results
P value Significance (BC) (BC) 0.001926 0.001614 0.117552
Yes Yes No
P value
Significance
IVF vs EP 0.001324 IVF vs IP 0.553812 IVF vs EVF 0.013062
Yes No Yes
P value Significance (BC) (BC) 0.007944 3.322872 0.078372
Yes No No
TABLE 6. EMG: Significance of the Results Lateral TA Subject P-value 1 2 3
0.032130 0.000655 /
Medial TA
Significance P value Yes Yes /
0.006910 / 0.073138
Significance Yes / No
TA muscles only for one subject due to the reduced compliance of the others. Thus, for the first subject both the muscles were analyzed, while for the second and the third subject only medial TA and lateral TA, respectively were considered. As for the results of the first subject, medial TA motor units were significantly more recruited in IVF compared to EVF, while lateral TA motor units were significantly more recruited in EVF compared to IVF. The third subject obtained similar results in the analysis of lateral TA muscle, which was significantly recruited more in EVF in comparison to IVF. No significant difference in the assessment of medial TA in the second subject was found, even though IVF turns were higher compared to EVF ones, as for the first subject (Table 6). DISCUSSION This first pilot study on IVF aims to carry out its anatomical and physiological features, to evaluate its effects on spoken and singing voice, to confirm its utility reported by professional voice users and the good results obtained after a first empirical application in patients with voice disorders. At the beginning of the project, the nomenclature matter was discussed. It is important to clarify that the research team decided to use the expression “Inspiratory Vocal Fry” for this new type of voice production exclusively referring to the perception of the glottal vibration pulses during the voice emission, as it happens with EVF, even though the effective anatomical and physiological characteristics of this type of phonation was unknown. As for videolaryngostroboscopy, false vocal folds adduction was significantly reduced in IVF compared to EVF, highlighting a balancing between adductor and abductor forces and a reduction of hyperkinetic attitude in IVF. These evidences were confirmed by the EMG results, which showed for the analyzed subjects a reduced activity in IVF
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of lateral TA, which directly influences false vocal folds movements. No significant difference was found between IVF and EP at a comfortable pitch and loudness, supporting the hypothesis that both these types of phonation are not characterized by a hyperkinetic attitude. Pharyngeal wall contraction values were significantly lower in IVF compared to EVF, meaning that configurational variations exist not only at laryngeal level, but also at pharyngeal level and confirming a nonhyperkinetic attitude in IVF. As for the comparison between IVF and EP, a significantly higher pharyngeal wall contraction in IVF was found, even though in this case the BC showed a nonsignificant difference. It can be hypothesized that in IVF the pharyngeal wall muscles maintain a tonic contraction without reaching the hyperkinetic attitude, which is typical of EVF. Vocal folds' stretching is significantly higher in IVF compared to EVF, because of the contraction of CT muscles which increase vocal folds stretching, elastic and nonhypertonic tension. For this analysis, EP was not compared to IVF and EVF because in this type of phonation, at a comfortable pitch and loudness, it is already known that there is not an increased activity of CT. Electroglottographic CQs were significantly higher in IVF compared to EVF and the other types of phonation highlighting a nontight adduction with elastic tension of the vocal muscle and, therefore, a reduced transglottic pressure gradient in IVF. Similar results were obtained considering CCQ, as IVF values for this parameter were significantly higher compared to EVF and EP, meaning that IVF is characterized by a more prolonged time of approach and separation between the free edges of the vocal folds and therefore a greater “massaging effect.” As regard EMG, medial TA motor units were more recruited in IVF, while lateral TA motor units were more recruited in EVF. According to these preliminary findings, it is possible to state that IVF is characterized by a clear phase difference in vibratory pattern between the mucosal layer, which freely vibrates, and the muscle-ligament one, which is static due to the elastic contraction of the medial TA. This anatomical configuration consequently allows a “massage” only for the mucosal layer. On the other hand, EVF is characterized by a low phase difference in vibratory pattern between muscle-ligament layer and mucosa, which simultaneously and compactly vibrate, due to medial TA relaxation. Nine subjects of the sample were not able to perform IVF at the first time. The following facilitating techniques, used empirically in everyday clinical practice, were successfully applied in order to achieve the correct production of IVF for all of them: starting the emission from the nose with closed lips and relaxed jaw, striving to produce the inspiratory sound quickly and strongly, protruding the tongue, reverse laugh, producing a very low note followed without interruption by an IP trying to maintain the same Fundamental Frequency (F0), and focusing on diaphragmatic activity. Considering the results of this study, similar properties between IVF and IP were found. As a matter of fact, as IP, IVF seems to be characterized by a synergy between
adductor and abductor muscles and a laryngeal lowering tendency. IVF can be described as a different vocal register in comparison to EVF, since it is associated with different laryngeal muscle activity, synergy, and anatomical configuration. Nevertheless, as previously mentioned, the expression “Inspiratory Vocal Fry” refers to the perception of the glottal vibration pulses during the voice emission. According to the results of this study, IVF can be hypothesized as a valid and safe technique since it improves glottic muscle elasticity and relaxation of supraglottic structures, reduces the hyperkinetic tendency, and allows an effective mucosal massage. Thus, in speech therapy it could be potentially useful in case of dysfunctional and organic dysphonias, postsurgical rehabilitation, and rehabilitation of the artistic voice, although further evidence is needed. For the same reasons, in vocal pedagogy and singing, it could be potentially suitable in vocal warm-up to facilitate the correct muscular and subglottic pressure balance, during the performance as a method to reduce muscular tension after fatiguing vocal tasks, in vocal cool-down after demanding performances, and to reduce frequent hyperfunctional behaviors typical of beginners. In this field, specific studies are desirable too. The limitations of the study are mostly related to the intrinsic properties of the pilot study. As regards the future perspectives, it could be useful to study what happens in case of vocal folds pathology and inflammation, the real effectiveness and applicability in the speech therapy of dysphonias and to improve the corpus of facilitating exercises. CONCLUSIONS The present study provides a preliminary insight on anatomical and physiological features of IVF, which is the voice production during inspiration of a sound with vocal fry perceptual characteristics. Considering IVF laryngeal muscle activity, synergy, and anatomical configuration highlighted in this study, it is possible to state that IVF is a different vocal register in comparison to EVF. The results of this project confirm that, as initially observed at a first empirical application on patients with voice disorders, IVF could be an excellent technique to reduce muscular hypertonic tension and to facilitate mucosal elasticity. It could be applied in speech therapy approach to dysfunctional and organic dysphonias, postsurgical treatment, in vocal pedagogy and practice of artistic voice. SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/10.1016/j. jvoice.2019.10.004. REFERENCES 1. Hollien H, Moore P, Wendhal R, et al. On the nature of vocal fry. J Speech Hear Res. 1966;9:245–247.
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