Professional Documents
Culture Documents
An Exploratory Study of Voice Change Associated With Healthy Speakers After Transcutaneous Electrical Stimulation To Laryngeal Muscles
An Exploratory Study of Voice Change Associated With Healthy Speakers After Transcutaneous Electrical Stimulation To Laryngeal Muscles
An Exploratory Study of Voice Change Associated With Healthy Speakers After Transcutaneous Electrical Stimulation To Laryngeal Muscles
Summary: Objectives. The purpose of this study was to determine if measurable changes in fundamental frequency
(F0) and relative sound level (RSL) occurred in healthy speakers after transcutaneous electrical stimulation (TES) as
applied via VitalStim (Chattanooga Group, Chattanooga, TN).
Study Design. A prospective, repeated-measures design.
Methods. Ten healthy female and 10 healthy male speakers, 20–53 years of age, participated in the study. All partic-
ipants were nonsmokers and reported negative history for voice disorders. Participants received 1 hour of TES while
engaged in eating, drinking, and conversation to simulate a typical dysphagia therapy protocol. Voice recordings
were obtained before and immediately after TES. The voice samples consisted of a sustained vowel task and reading
of the Rainbow Passage. Measurements of F0 and RSL were obtained using TF32 (Milenkovic, 2005, University of
Wisconsin). The participants also reported any sensations 5 minutes and 24 hours after TES.
Results. Measurable changes in F0 and RSL were found for both tasks but were variable in direction and magnitude.
These changes were not statistically significant. Subjective comments ranged from reports of a vocal warm-up feeling to
delayed onset muscle soreness.
Conclusions. These findings demonstrate that application of TES produces measurable changes in F0 and RSL. How-
ever, the direction and magnitude of these changes are highly variable. Further research is needed to determine factors
that may affect the extent to which TES contributes to significant changes in voice.
Key Words: Transcutaneous electrical stimulation–Percutaneous electrical stimulation–Muscle fatigue–Delayed
onset muscle injury.
INTRODUCTION Although the use of TES is new to voice therapy regimes, the
The use of electrotherapy for treating physical ailments can be practice of applying electrical stimulation to laryngeal muscles
traced back to 46 AD when a Roman physician used the shock is not new. The feasibility of using percutaneous electrical
from electric eels to treat headaches and gout. Electrotherapy stimulation (PES) to improve contraction in select intrinsic
has since endured cyclical popularity.1 In 1961, Liberson et al laryngeal muscles was first suggested by Zealear and Dedo4
demonstrated the possible benefits of using electrical stimula- in 1977 after they successfully reanimated paralyzed laryngeal
tion to improve the gait of hemiplegic patients.2 This introduc- muscles in canines. Subsequent animal studies in the field of
tion by Libeson et al marked the beginning of the current otolaryngology have demonstrated the effectiveness of PES in
widespread use of a variety of electrical therapy techniques, in- restoring abduction and adduction in paralyzed laryngeal
cluding transcutaneous electrical stimulation (TES), in the muscles.5–7 Applications of PES to laryngeal muscles in
rehabilitation of weakened skeletal muscles. In contrast, the humans include using an implantable device on the posterior
use of TES to treat swallowing and voice disorders by cricoarytenoid muscle to help maintain glottal opening in cases
speech-language pathologists (SLPs) is relatively new.3 Clini- of bilateral vocal fold paralysis8 and using electrical implants to
cians who use TES to treat dysphagia have given anecdotal control the laryngeal spasms of abductor spasmodic dysphonia
reports of perceptual voice changes in their patients (VitalStim by stimulating the thyroarytenoid or lateral cricoarytenoid mus-
Training, Atlanta, Georgia, 2004). Consequently, these clini- cles.9 Although current and future developments in PES are
cians have begun using TES to treat a variety of voice disorders promising, the procedure is invasive and not widely used. By
in the absence of coexisting dysphagia. contrast, TES offers a noninvasive and cost-effective method
to treat selected voice disorders; however, there is a lack of em-
pirical evidence regarding its effectiveness.
Clinicians using TES to facilitate perceptual changes have
Accepted for publication July 21, 2009.
A portion of this research was presented at the 35th Annual Voice Symposium, titled
provided anecdotal reports about the effectiveness of TES to tar-
Voice Change in Normal Speakers Associated with Surface Electrical Stimulation, Phila- get voice by using two of the six electrode placement patterns
delphia, PA, June 2006.
From the *Department of Educational Psychology and Special Education, Georgia State
suggested by VitalStim (VitalStim Training). Patterns 3a and
University, Atlanta, Georgia; yDepartment of Communication Sciences and Disorders, 3b have been touted as being more likely to elicit perceptual
Valdosta State University, Valdosta, Georgia; and the zEmory Voice Center, Emory Uni-
versity, Atlanta, Georgia.
voice changes (Figure 1). Both of these patterns involve placing
Address correspondence and reprint requests to Linda P. Fowler, Educational Psychol- bipolar electrodes superior to the hyoid bone and superior to the
ogy and Special Education, Georgia State University, P.O. Box 3979, Atlanta, GA
30302-3979. E-mail: lpfowler@gsu.edu
thyroid notch. According to proponents, these patterns are more
Journal of Voice, Vol. 25, No. 1, pp. 54-61 likely to recruit cricothyroid muscle fibers and thus, increase
0892-1997/$36.00
Ó 2011 The Voice Foundation
glottal closure. To further increase the likelihood of recruiting
doi:10.1016/j.jvoice.2009.07.006 cricothyroid fibers, proponents have recommended placing one
Linda P. Fowler, et al Voice Change After TES to Laryngeal Muscles 55
set of bipolar electrodes directly over the cricothyroid muscles in refrain from resisting any pitch changes that occurred as the in-
what can be termed a modified 3b pattern (VitalStim Training). tensity of the electrical current was increased. Comparisons
The effectiveness of cricothyroid electrode placement to im- were made between the beginning and ending F0 levels. Similar
prove voice quality by increasing glottal closure is untested. to the findings reported by Vilkman et al,18 some subjects dis-
The claims of increased glottal closure are also questionable played increases in F0 as the current amplitude increased while
considering the well-known fact that contraction of the crico- others displayed decreases.19 The results of this study raised
thyroid lengthens the vocal folds. Empirical findings related the question regarding what acoustic changes occurred in the
to the extent of intrinsic muscle recruitment from TES can be voice after an hour of TES, because research has shown that
gleaned from studies that investigated the effects of using most SLPs apply TES to the neck for an hour when treating
TES to treat dysphagia. Recent studies that paired TES with dysphagia.20
videofluoroscopy reported evidence of electrical current pene- The current lack of knowledge regarding the effects of TES
tration to sternohyoid (SH) muscle; however, no evidence of on voice production, coupled with increasing anecdotal reports
penetration to intrinsic laryngeal muscles was found in normal of TES use with voice disorders, prompted this research. The
volunteers10 or in patients with dysphagia.11 A study conducted purpose of this exploratory study was to determine if measur-
by Humbert et al paired TES with videonasolaryngoscopic re- able trends of fundamental frequency (F0) and sound level
cordings.12 A statistically significant reduction in the angle of (SL) occurred in healthy volunteers after an hour of TES. F0
the anterior commissure was reported when a single channel and SL measurements are often used clinically to judge changes
of bipolar electrodes was placed in the submental region of in voice associated with treatment or conditions that may affect
the neck. The researchers concluded that the amount of vocal the voice, that is, vocal fold lesions, prolonged vocal use, vocal
fold closure was not sufficient to prevent aspiration. Another fatigue, and others. F0 is an acoustic measure of the frequency
electrode placement pattern explored by Humbert et al resulted of the vocal fold vibrations. Vibratory frequency results from an
in an increase in vocal fold closure when bipolar electrodes interplay between vocal fold length, mass, tension, and outgo-
were positioned above the hyoid bone vertically down to the cri- ing airflow rates.21–25 Both intrinsic and extrinsic muscles can
coid cartilage. At first glance, the results from Humbert et al ap- be involved in vocal fold adjustments. Vocal loudness, or SL,
peared to support TES recruitment of intrinsic laryngeal is also controlled by an interplay of physical factors that include
muscles. However, their results may reflect recruitment of the degree of glottal resistance imposed by the vocal folds to
neck strap muscles, as results from other human and animal outgoing airflow, the level of subglottal pressures required to
studies have shown that PES applied to various strap muscles overcome glottal resistance, the velocity of vocal fold closure
during surgical operations effected changes in glottal opening and changes in the rate of the airflow pulse at closure.26–31
and fundamental frequency (F0).13–17 Vilkman et al18 reported Given that TES applied to the neck will cause extrinsic, and
in a meta-analysis that PES applied to the SH and sternothyroid possibly intrinsic muscles to contract, any changes in the voice
(ST) indirectly raised F0 in some studies and lowered F0 in would likely be reflected in either F0 or SL.
other studies. The disparity between the direction of F0 change This study was purely exploratory in nature because of the
was attributed to a variety of factors including, but not limited lack of previously published empirical findings concerning
to, head position; tracheal pull; whether SH and/or ST were the effects of TES on vocal acoustics. As such, the researchers
stimulated singularly, simultaneously, or when paired with made no hypotheses regarding the results.
other muscles; and reflex responses in muscles not directly
stimulated. The extent to which TES can effect similar vocal
changes has not been fully investigated. MATERIALS AND METHODS
In an unpublished study by the authors, TES was applied to Participants
the necks of healthy speakers. The current amplitude was in- Ten healthy female (F) and 10 healthy male (M) speakers
creased in 0.5-milliamperes (mA) increments per second while (n ¼ 20) between 20 and 53 years of age (mean age ¼ 26 years)
the speakers sustained various vowel sounds. Participants were participated in this study. All participants were nonsmokers and
instructed to begin phonating at a comfortable pitch level and to reported negative histories for voice, speech, phonological,
56 Journal of Voice, Vol. 25, No. 1, 2011
Voice recordings
Pre- and posttreatment voice recordings were collected in
a sound-attenuated booth. Voice recordings were obtained us-
ing an omni-directional microphone (Audio Techinca #3032,
Stow, OH) connected to a preamplifier (M-AudioMobilePre
USB, Irwindale, CA), at a mouth-to-microphone distance of
30 cm.33 This recording procedure allowed for F0 and relative
sound level (RSL) measurements. The voice samples were dig-
itized directly into a desktop PC. Each participant produced the
FIGURE 2. Posttreatment F0 and RSL changes for sustained vowel vowel /a/ three times for approximately 3–5 seconds, and read
production. the first two sentences of the Rainbow Passage (RP)34 three
times. Participants were instructed to produce the sentences at
neurological, psychiatric, and swallowing disorders. All partic- comfortable effort and natural pitch levels.
ipants were free of voice complaints on the day of testing. An
SLP with 20 years of experience in the evaluation and treatment Subjective participant comments
of voice disorders perceptually judged that voice quality was Participants were asked to provide comments regarding the sen-
normal on the day of testing. Hearing acuity for all participants sations they felt in the laryngeal area 5 minutes after the post-
was judged to be within normal limits for the reception of con- treatment voice recordings and again 24–48 hours after data
versational speech. collection to determine the presence of fatigue and/or delayed
onset muscle soreness (DOMS). DOMS is characterized by ten-
Procedures derness, dull aching pain, and stiffness in muscles 24–48 hours
TES was applied using VitalStim (Chattanooga Group, Chatta- after unaccustomed exercise.35–38
nooga, TN). The skin in the laryngeal and submental areas was
cleaned with alcohol, and wiped with TENS Clean-Cote Skin Data analysis
Wipes (Tyco Unit-Patch Model UP220; Uni-Patch, Wabasha, The digitized voice samples were analyzed using TF32, ‘‘a
MN) to increase adherence of the bipolar electrodes to the time-frequency analysis software program for 32-bit Windows
skin. Additionally, all male participants were clean shaven to (95/98/NT/2000/XP) for the analysis of speech and other audio-
ensure adequate electrode adhesion. Adult-sized bipolar elec- frequency waveforms.’’39 F0 was derived from the middle 1 sec-
trodes (VitalStim REF 59000; Chattanooga Group, Chatta- ond of each vowel phonation. RSL for the sustained vowels was
nooga, TN) with a 2.1-cm diameter and a 3.46-cm2 active also determined by using the middle 1-second segment to deter-
area were positioned lateral to midline in the submental region mine the average root mean square of the energy. Analysis of F0
and in the lateral cricothyroid spaces. This electrode placement and RSL of the connected speech samples were determined in
corresponded to modified 3a and 3b positions suggested by Vi- a similar manner used for vowel analysis with the exception
talStim trainers (VitalStim Training). The VitalStim device had that the entire sentence production was analyzed. Each acoustic
a fixed 80-Hz pulse rate and emitted fixed biphasic pulse dura- measure was averaged across the three vowels and spoken sen-
tions of 700 microseconds. The intensity was gradually in- tences for each speaker and entered as one data point per
creased in 0.5-mA increments until participants reported speaker.
feeling a ‘‘grabbing’’ sensation. As per the Training Manual
for Patient Assessment and Treatment Using VitalStim Electri- Statistical analysis
cal Stimulation,32 this ‘‘grabbing’’ sensation was associated Twenty-four randomly selected voice recordings representing
with muscle contraction and reflected the minimum ‘‘motor’’ 20% of the data, evenly distributed across the four recording
level of stimulation for each participant. Stimulation was ap- conditions, were reanalyzed using TF32 to determine intrarater
plied at the minimum motor level for 1 hour as per the standard and interrater measurement reliability. Pearson product-moment
VitalStim dysphagia protocol recommendation. The VitalStim reliability coefficients were calculated between the measure-
device automatically cycled off 1 second each minute through- ments obtained by the first and second investigators. Interrater
out the hour. Participants gradually increased the intensity, reliability (r) for F0 and RSL of vowels and spoken sentences
when needed, to maintain the ‘‘grabbing’’ sensation throughout ranged from 0.98 to 1.00 (P < 0.000).
the entire hour of treatment. This protocol was consistent with
recommendations made by VitalStim educational trainers (Vi- RESULTS
talStim Training). Participants engaged in conversational Figures 2 and 3 demonstrate posttreatment changes in mean F0
speech, ate and drank during the treatment session. for both of the vocal tasks. Posttreatment changes in F0 means
To determine if the degree of cutaneous adipose tissue was re- for all participants ranged from 20.6 to 31.27 Hz for /a/ and
lated to voice changes with the use of TES, skin fold measure- from 5.61 to 20.93 Hz for the RP. Results of independent-
Linda P. Fowler, et al Voice Change After TES to Laryngeal Muscles 57
TABLE 1.
Participants Divided Into Groups Based on Posttreatment Sensory Sensations, Current Amplitude, Neck Fat, Sensations 5
Minutes After TES, and Sensations 27–48 Hours After TES
F0 RSL
Current Sensations 5 min Sensations 24/48 hr
Part Amplitude Neck Fat After TES After TES /a/ RP /a/ RP
Group 1: warm-up
F3 4.5–6.5 4.33 Pitch seemed higher, noticed Three twitches later + + +
a ‘‘warm-up’’ feeling the same night
F6 6–7 7.00 Voice sounded lower in pitch. No sensation + + +
F7 6–8 6.83 Neck felt loose; voice sounded No sensation + + + +
a little clearer
M2 4.5–10 2.17 Noticeable contractions in chest No sensations
during TES; no sensations
afterward
M5 4.5–7 3.67 Neck felt slightly less tense. No sensations + +
No change in voice
M10 4.5–9.5 2.00 Easier to maintain sounds Muscles in neck felt more relaxed + +
Group 2: fatigue
F1 4.5–8.5 13.50 Voice felt higher and less nasal; Voice continued to feel ‘‘a little + + + +
neck felt tighter; ‘‘voice tight’’ that same night
felt more closed’’
F10 4–7.5 4.17 Voice sounded clearer, felt No sensations + + +
‘‘rejuvenated.’’ Neck felt stiff on
the sides and sore for 30 min
M3 5–8 3.83 Head movements felt like different No sensations + +
muscles needed to be used;
neck felt loose and stretched out
M6 5–7.5 6.83 Felt a little numbness No sensations + +
and slight tingling
M7 4–16 2.50 Neck felt tired; felt sensation No sensations + + +
of choking during stimulation
M8 4.5–22.5 3.67 Neck felt tired; more relaxed; Neck felt more relaxed
voice sounded clearer
M9 3.5–8.5 2.00 No change in voice or neck; No sensation + + + +
frequently needed
to clear throat
Group 3: delayed onset muscle soreness
F2 4.5–8 12.30 Twitching and tingling under Soreness on left side under chin + + +
chin that lasted about 30 min
F4 5.5–9 13.50 Some tingling Neck muscles feel like they +
have been through a workout
F5 5–10 2.83 Numb spot on neck Voice seems to be husky. +
Neck muscles feel like they have
been through a workout
F8 4.5–10 9.33 Voice smoother and clearer; No change in voice; + + + +
neck felt relaxed neck quite sore
F9 4.5–7.5 3.67 Skin felt raw Neck felt sore as after a workout + + +
M1 5–7 3.17 Neck felt tired; muscles been Throat felt sore during swallows + +
through workout
M4 4.5–7.5 6.50 Neck felt fatigued, as if subjected Not very sore the next day, but on + +
to talking for a long duration the second day, very sore.
+: Indicates a posttreatment increase; : indicates a posttreatment decrease.
Abbreviation: RP, Rainbow Passage.
subsequent investigations should include laryngoscopic Muscle fatigue has been described as a ‘‘failure to maintain
evaluations to verify vocal health before applying TES. the required or expected force’’ after repeated activity.55 The
It has long been known that skeletal muscles fatigue more rap- rapid fatigue associated with TES has been attributed to
idly from electrically induced than volitional contractions.53,54 synchronous recruitment of the motor units, imprecise motor
Linda P. Fowler, et al Voice Change After TES to Laryngeal Muscles 59
3. What current amplitude levels should be applied to pre- 16. Kotby MN, Haugen LK. Attempts at evaluation of the function of various
vent muscle fatigue and/or DOMS? laryngeal muscles in the light of muscle and nerve stimulation experiments
in man. Acta Otolaryngol. 1970;70:419–427.
4. Should TES be used simultaneously with vocal exercises 17. Sapir S, Campbell C, Larson C. Effect of geniohyoid, cricothyroid, and ster-
or should it not be applied during vocal production? nothyroid muscle stimulation on voice fundamental frequency of electrically
5. If voice exercises can be paired with TES, which ones elicited phonation in rhesus macaque. Laryngoscope. 1981;91:457–468.
will be the most effective and safe? 18. Vilkman E, Sonninen A, Hurme P, Körkkö P. External laryngeal frame
6. What types of voice disorders are most appropriate to in- function in voice production revisited: a review. J Voice. 1996;10:78–92.
19. Gorham-Rowan M, Fowler L, Hapner ER. A Tutorial on Muscle Function
clude TES as a treatment modality? and the Effects of Surface Electrode Stimulation on Voice. Atlanta, GA:
7. Is hypertrophy in extrinsic laryngeal muscles a desired Georgia Speech-Language-Hearing Association Convention; March 2006.
outcome when treating some voice disorders? 20. Crary MA, Carnaby-Mann GD, Faunce BA. Electrical stimulation therapy
for dysphagia: descriptive results of two surveys. Dysphagia. 2007;22:
Review of the participants’ comments from 24 hours after 165–173.
21. Perlman AL, Titze IR, Cooper DS. Elasticity of canine vocal fold tissue. J
their TES sessions reinforced the importance of investigating Speech Hear Res. 1984;27:212–219.
the possible positive and deleterious effects of TES through 22. Perlman AL, Titze IR. Developmental of an in vitro technique for measuring
the aforementioned questions. In addition, this study’s data elastic properties of vocal fold tissue. J Speech Hear Res. 1988;31:288–298.
were from participants with healthy voices, and as such, the 23. Colton RH. Physiological mechanisms of vocal frequency control: the role
muscle and sensory responses of people with diagnosed voice of tension. J Voice. 1988;2:208–220.
24. Van den Berg J, Tan TS. Results of experiments with human larynges. Prac-
disorders could be dissimilar to the findings reported here. tica Oto-Rhino-Laryngol. 1959;21:425–450.
The results from this study demonstrate the need for further em- 25. Allen EL, Hollien H. A laminagraphic study of pulse (vocal fry) register
pirical investigation before TES is adopted as a common ap- phonation. Folia Phoniatr Logop. 1973;25:241–250.
proach SLPs use to treat voice disorders. 26. Isshiki N. Regulatory mechanism of voice intensity regulation. J Speech
Hear Res. 1964;7:17–29.
27. Isshiki N. Vocal intensity and air flow rate. Folia Phoniatr Logop. 1965;17:
REFERENCES 92–104.
1. Mannheimer JS, Lampe GN. Clinical Transcutaneous Electrical Nerve 28. Ladefoged P, McKinney NP. Loudness, sound pressure and subglottal pres-
Stimulation. Philadelphia: F.A. Davis Company; 1984. 1. sure in speech. J Acoust Soc Am. 1963;35:454–460.
2. Liberson WT, Holmquest HJ, Scott D, Dow M. Functional electrotherapy: 29. Sundberg J, Titze IR, Scherer R. Phonatory control in male singing: a study
stimulation of peroneal nerve synchronized with the swing phase of the gait of the effects of subglottal pressure, fundamental frequency, and mode of
of hemiplegia patients. Arch Phys Med Rehabil. 1961;42:101–105. phonation on the voice source. J Voice. 1993;7:15–29.
3. Freed ML, Freed L, Chatburn RL, Christian M. Electrical stimulation for 30. Titze IR. Principles of Voice Production. Englewood Cliffs: Prentice-Hall
swallowing disorders caused by stroke. Respir Care. 2001;46:466–474. Inc; 1994. 226–227.
4. Zealear DL, Dedo HH. Control of paralyzed axial muscles by electrical 31. Titze IR, Sundberg J. Vocal intensity in speakers and singers. J Acoust Soc
stimulation. Acta Otolaryngol. 1977;83:514–527. Am. 1992;91:2936–2946.
5. Obert PM, Young KA, Tobey DN. Use of direct posterior cricoarytenoid 32. Wijting Y, Freed M. Training Manual for Patient Assessment and Treatment
stimulation in laryngeal paralysis. Arch Otolaryngol. 1984;110:88–92. Using VitalStim Electrical Stimulation. Hixon, TN: Chattanooga Group;
6. Bergmann K, Warzel H, Eckhardt HU, Hopstock U, Hermann V, 2004. 70.
Gerhardt HJ. Long-term implantation of a system of electrical stimulation 33. Titze IR, Winholtz WS. Effect of microphone type and placement on voice
of paralyzed laryngeal muscles in dogs. Laryngoscope. 1988;98:455–459. perturbation measures. J Speech Hear Res. 1993;36:1177–1190.
7. Sanders I. Electrical stimulation of laryngeal muscle. Otolaryngol Clin 34. Fairbanks G. Voice and Articulation Drillbook. 2nd ed).. New York: Harper
North Am. 1991;24:1253–1274. & Row; 1960. 124–139.
8. Zealear DL, Billante CR, Courey MS, Sant Anna GD, Netterville JL. Elec- 35. Hough T. Ergographic studies in muscular soreness. Am J Phys. 1902;7:
trically stimulated glottal opening combined with adductor muscle botox 76–92.
blockade restores both ventilation and voice in a patient with bilateral la- 36. Armstrong RG. Mechanisms of exercise-induced delayed onset muscular
ryngeal paralysis. Ann Otol Rhinol Laryngol. 2002;111:500–506. soreness: a brief review. Med Sci Sports Exerc. 1984;16:529–538.
9. Bidus KA, Thomas GR, Ludlow CL. Effects of adductor muscle stimulation on 37. Armstrong RB, Garshnek V, Schwane J. Muscle inflammation: response to
speech in abductor spasmodic dysphonia. Laryngoscope. 2000;110: eccentric exercise. Med Sci Sports. 1980;12:94–102.
1943–1949. 38. Bobbert MF, Hollande AP, Huijing PA. Factors in delayed onset soreness of
10. Humbert IA, Poletto CJ, Saxon KG, et al. The effect of surface electrical man. Med Sci Sports Exerc. 1986;18:75–81.
stimulation on hyo-laryngeal movement in normal individuals at rest and 39. Sherman D, Jensen PJ. Harshness and oral-reading time. J Speech Hear
during swallowing. J Appl Physiol. 2006;101:1657–1663. Disord. 1962;27:172–177.
11. Ludlow CL, Humbert I, Saxon K, Poletto C, Sonies B, Crujido L. Effects of 40. Rantala L, Vilkman E. Relationship between subjective voice complaints and
surface electrical stimulation both at rest and during swallowing in chronic acoustic parameters in female teachers’ voices. J Voice. 1999;13:484–495.
pharyngeal dysphagia. Dysphagia. 2007;22:1–10. 41. Safran MR, Seaber AV, Garrett WE Jr. Warm-up and muscular injury pre-
12. Humbert IA, Poletto CJ, Saxon KG, Kearney PR, Ludlow CL. The effect of vention. An update. Sports Med. 1989;8:239–249.
surface electrical stimulation on vocal fold position. Laryngoscope. 42. Stemple JC, Stanley J, Lee L. Objective measures of voice production in
2008;118:14–19. normal subjects following prolonged voice use. J Voice. 1995;9:127–133.
13. Erickson D, Baer T, Harris KS. The role of the strap muscles in pitch low- 43. Vintturi J, Alku P, Sala E, Sihvo M, Vilkman E. Loading-related subjective
ering. In: Bless DM, Abbs JH, eds. Vocal Fold Physiology: Contemporary symptoms during a vocal loading test with special reference to gender and
Research and Clinical Issues. San Diego: College-Hill; 1983:279–285. some ergonomic factors. Folia Phoniatr. 2003;55:55–69.
14. Faaborg-Andersen K, Sonninen A. The function of the extrinsic laryngeal 44. Titze IR, Hunter EJ, Svec JG. Voicing and silence periods in daily and
muscles at different pitch: an electromyographic and roentgenologic inves- weekly vocalizations of teachers. J Acoust Soc Am. 2007;121:469–478.
tigation. Acta Otolaryngol. 1960;51:89–93. 45. Gelfer MP, Andrews ML, Schmidt CP. Effects of prolonged loud reading
15. Sonninen A. The role of the external laryngeal muscles in length-adjustment on selected measures of vocal function in trained and untrained singers.
of the vocal cords in singing. Acta Otolaryngol. 1956;Suppl 130: 1–102. J Voice. 1991;5:158–167.
Linda P. Fowler, et al Voice Change After TES to Laryngeal Muscles 61
46. Novak A, Dlouha O, Capkova B, Vohradnik M. Voice fatigue after theatre 56. Peckham PH, Knutson JS. Functional electrical stimulation for neuromus-
performance in actors. Folia Phoniatr. 1991;43:74–78. cular applications. Annu Rev Biomed Eng. 2005;7:327–360.
47. Buekers R, Bierens E, Kingma H, Marres EH. Vocal load as measured by 57. Sciote JJ, Horton MJ, Rowlerson AM, Link J. Specialized cranial muscles:
the voice accumulator. Folia Phoniatr Logop. 1995;47:252–261. how different are they from limb and abdominal muscles. Cells Tissues Or-
48. Lauri ER, Alku P, Vilkman E, Sala E, Sihvo M. Effects of prolonged oral gans. 2003;174:73–86. 40.
reading on time based glottal flow waveform parameters with special refer- 58. National Skeletal Muscle Research Center Web site. Muscle physiology
ence to gender differences. Folia Phoniatr Logop. 1997;49:234–246. home page. 2008. Available at: http://muscle.ucsd.edu/NSMRC/home.
49. Rantala L, Lindholm P, Vilkman E. F0 changes due to voice loading in lab- shtml. Accessed October 18, 2008.
oratory and field conditions: a pilot study. Logoped Phoniatr Vocol. 59. Korfage JAM, Schueler YT, Brugman P, Van Eijden TMGJ. Differences in
1998;23:164–168. myosin heavy-chain composition between human jaw-closing muscles and
50. Vilkman E, Lauri ER, Alku P, Sala E, Sihvo M. The effects of prolonged supra- and infrahyoid muscles. Arch Oral Biol. 2001;46:821–827.
reading on F0, SPL, subglottal pressures and amplitude characteristics of 60. Ludlow C. Electrical stimulation and dysphagia: what we do and don’t
glottal flow waveform. J Voice. 1999;13:305–315. know. ASHA Leader. 2008;13:8–11.
51. Laukkanen AM, Jarvinen K, Artkoski M, et al. Changes in voice and sub- 61. McArdle WD, Katch FI, Katch VL. Essentials of Exercise Physiology. 2nd
jective sensations during a 45-min vocal loading test in female subjects with ed).. Philadelphia, PA: Lippincott Williams & Wilkins; 2000.
vocal training. Folia Phoniatr Logop. 2004;56:335–346. 62. Hagerman FC, Hikida RS, Staron RS, Sherman WM, Costill DL. Muscle
52. Laukkanen AM, Ilomaki I, Leppanen K, Vilkman E. Acoustic measures damage in marathon runners. Physician Sports Med. 1984;12:39–48.
and self-reports of vocal fatigue by female teachers. J Voice. 2008;22: 63. Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced
283–289. muscle fibre injury. Sports Med. 1991;12:184–207.
53. Marsolais EB, Edwards BG. Energy costs of walking and standing with 64. Howell JN, Chleboun G, Conatser R. Muscle stiffness, strength loss, swell-
functional neuromuscular stimulation and long leg braces. Arch Phys ing and soreness following exercise-induced injury in humans. J Physiol.
Med Rehabil. 1988;69:243–249. 1993;464:183–196.
54. Riener R. Model-based development of neuroprosthesis for paraplegic pa- 65. Yu J, Carlsson L, Thornell LE. Evidence for myofibril remodeling as op-
tients. Philos Trans R Soc Lond B Biol Sci. 1999;354:877–894. posed to myofibril damage in human muscles with DOMS: an ultrastruc-
55. Edwards RHT. Human muscle function and fatigue. Ciba Found Symp. tural and immunoelectron microscopic study. Histochem Cell Biol.
1981;82:1–18. 2004;121:219–227.