Metabolic Mechanisms of Vocal Fatigue

*Chayadevie Nanjundeswaran, †,‡Jessie VanSwearingen, and §,‖,¶,#,**Katherine Verdolini Abbott, *Johnson City,
Tennessee, and †‡§‖¶#**Pittsburgh, Pennsylvania

Summary: Objective. This study aimed to identify potential metabolic mechanisms including (1) neuromuscular
inefficiency, (2) cardiovascular recovery deficits, or (3) both, in individuals with complaints of vocal fatigue.
Study Design. Within- and between-subjects group design was used in this study.
Methods. Three groups of women participated in the study, including (1) individuals with complaints of vocal fatigue;
(2) vocally healthy sedentary individuals; and (3) vocally healthy, cardiovascularly conditioned individuals. Group as-
signment was based on results from the Vocal Fatigue Index, laryngeal examination, and self-report regarding exercise
regimens. Metabolic profiles were obtained using gas exchange measures monitored during vocal task performance
(reading) at two different loudness levels, and during recovery from reading.
Results. Statistical analyses did not reveal reliable group differences in metabolic cost for or recovery from vocal
tasks. However, descriptive review of oxygen uptake and recovery kinetics revealed patterns indicating reliance on dif-
ferential energy resources for the vocal task in individuals with vocal fatigue compared with cardiovascularly trained,
vocally healthy individuals in particular. Slow oxygen uptake kinetics at task onset was a characteristic of the vocal
fatigue group, indicating a general reliance on anaerobic resources to meet the demands of the vocal task, pointing to
possible neuromuscular inefficiency. Individuals with vocal fatigue also demonstrated an increase in oxygen consump-
tion following vocal task compared with cardiovascularly trained individuals, suggesting possible cardiovascular recovery
deficits.
Conclusion. This study provides initial data relevant to possible metabolic mechanisms of vocal fatigue and the po-
tential relevance of aerobic conditioning in individuals with such fatigue.
Key Words: Vocal fatigue–Gas exchange–Neuromuscular inefficiency–Aerobic conditioning–Oxygen uptake kinetics.

INTRODUCTION
Vocal fatigue is a frequently occurring, often debilitating con-
dition, affecting many individuals with voice problems.
Professional and other voice users may be susceptible to this
fatigue, which may affect social and occupational functioning.1–3
Prior research has attempted to identify mechanisms underly-
ing vocal fatigue and possible treatment options for it. However,
interpretation of results has been complicated by the lack of a
consistent definition of vocal fatigue itself and by the use of dif-
ferent study methodologies including (1) study of individuals
with and without vocal complaints,1,4–6 (2) study of voice changes
following prolonged voice use,7–11 (3) study of treatment out-
comes for individuals with complaints of vocal fatigue,2,12–14 and
(4) study of recovery from vocal loading in healthy individuals.15
Moreover, existing data have failed to reveal a robust relation-
ship across self-reported and instrumented measures of vocal
fatigue, thereby providing minimal information about mecha-
Accepted for publication September 13, 2016.
Preliminary data were presented at the 36th Symposium: Care of the Professional Voice,
Philadelphia, Pennsylvania, 2007; the Fall Voice Conference, Atlanta, Georgia, 2013; and the
annual American Speech-Language-Hearing Association Convention, Denver, Colorado, 2015.
From the *Department of Audiology and Speech-Language Pathology, East Tennessee
State University, Johnson City, Tennessee; †Department of Physical Therapy, University
of Pittsburgh, Pittsburgh, Pennsylvania; ‡School of Nursing, University of Pittsburgh, Pitts-
burgh, Pennsylvania; §Department of Communication Sciences and Disorders, University
of Pittsburgh, Pittsburgh, Pennsylvania; ‖Department of Otolaryngology, University of Pitts-
burgh, Pittsburgh, Pennsylvania; ¶McGowan Institute for Regenerative Medicine, University
of Pittsburgh, Pittsburgh, Pennsylvania; #Center for the Neural Basis of Cognition, Carnegie-
Mellon University, Pittsburgh, Pennsylvania; and the **Center for the Neural Basis of
Cognition, University of Pittsburgh, Pittsburgh, Pennsylvania.
Address correspondence and reprint requests to Chayadevie Nanjundeswaran, Department
of Audiology and Speech-Language Pathology, College of Clinical and Rehabilitative Health
Sciences, East Tennessee State University, Lamb Hall, Box 70643, Johnson City, TN 37614.
E-mail: nanjundeswar@etsu.edu
Journal of Voice, Vol. 31, No. 3, pp. 378.e1–378.e11
0892-1997
© 2017 The Voice Foundation. Published by Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.jvoice.2016.09.014
nisms that may underlie this phenomenon. In sum, mixed and
inconclusive results in the vocal fatigue literature are attribut-
able to uncertainties about the definition of vocal fatigue,
variations in the choice of subject populations across studies,
the use of varying instrumented and self-report measures that
may not be sensitive to capture this variegated phenomenon, and
the use of different loading tasks that may or may not elicit vocal
fatigue.16 Given the debilitating nature and prevalence of this
condition,2,3 it is imperative to conduct further probes to under-
stand the underlying mechanisms and identify effective treatment
options.
In contrast to the situation in the literature on vocal fatigue,
research on fatigue in the exercise physiology domain has been
more extensive. Fatigue has been investigated under three schools
of thought: schools that emphasize peripheral fatigue, those that
emphasize central fatigue, and those that emphasize a combi-
nation of peripheral and central mechanisms. In each school of
thought, fatigue has been variably defined and different causes
of fatigue have been proposed.17–25 Full discussion is beyond the
scope of this paper. However, in brief, peripheral fatigue is thought
to result from factors relating to the neuromuscular junction and
muscle function itself, including factors pertaining to the intra-
cellular environment and muscle fibers.17,21,22 In contrast, central
fatigue is associated with reduced recruitment of motor units,
poor coordination of recruited motor units, and reduced central
drive due to increased inhibitory input to the motor cortex.25,26
The third school of thought emphasizes the interplay between
central and peripheral mechanisms.18,24,27 Among hypotheses, a
common proposal is that in both peripheral and central fatigue,
the oxygen supply to the muscle and the brain is inadequate for
the task demands.28 In sum, oxygen is needed to meet the energy
demands of active tissues during physical activity or task
Chayadevie Nanjundeswaran, et al Vocal Fatigue 378.e2

TABLE 1.
Oxygen Supply Issues in Fatigue

• Oxygen supply may be altered or inadequate due to inadequate delivery of oxygen to the working muscles (related to
cardiac output and circulation issues), and extraction of oxygen from blood delivered to the working muscle may be
inadequate to support the physical activity—the opposite of endurance,25
• There can be increased reliance on anaerobic resources during task performance due to a delay in the timing of the
oxygen supply to meet task demands. The result is a depletion of the local (muscle) anaerobic energy resources (PCr,
glycogen) followed by excessive metabolite accumulation (eg, lactic acid, hydrogen ions, and calcium ions), the by-
products of anaerobic metabolism. The accumulation of these metabolites impacts both muscle physiology and
neuromuscular function, which in turn can contribute to a decline in force production or inefficient patterns of muscle
recruitment for a task.25,26 (Note that in the presence of oxygen, some of the accumulated metabolites can be used as
fuel in aerobic metabolism; for information about the Krebs cycle, see Ref. 33),
• Inadequate supply of oxygen for the energy demand influences inhibitory feedback to the CNS and may contribute to
the perception of effort in task performance,23
• Endurance exercise, which is known to enhance oxygen supply (due to improved cardiac output and oxygen
extraction), has been shown to delay the onset of fatigue, presumably due to the provision of adequate oxygen to
meet task demands earlier in the onset of performance, and thus the reduction or prevention of the accumulation of
excessive metabolites.27,28
CNS, central nervous system; PCr, creatine phosphate.

performance. The desired energy source for this activity is aerobic
metabolism, which is dependent on an adequate and consistent
supply of oxygen to the active tissues. With fatigue there may
be a lag in availability or poor extraction of oxygen to meet task
demands. When oxygen supply is insufficient, task-related
fatigue—defined as performance decrements over time—may
ensue.
Despite the desired use of aerobic metabolism to meet task-
related energy demands, at the onset of physical activity, there
is an initial reliance on anaerobic metabolism as an energy source.
Specifically at the onset of activity, reliance is on local tissue
stores of creatine phosphate and glycogen in the muscle to meet
task demands. These fuel sources can independently support per-
formance for a few minutes only. Continued performance is
sustained by aerobic metabolism, which is dependent on an ad-
equate supply of oxygen to the tissues, as oxygen is the fuel
needed for aerobic metabolism (ie, aerobic resources). Mis-
match between oxygen supply to the active tissues and energy
demands can lead to performance decrements, that is, fatigue23,29–32
A summary of mechanisms related to oxygen supply in fatigue
is provided in Table 1.
Relative to oxygen supply, two specific potential mecha-
nisms may explain fatigue: (1) neuromuscular inefficiency, and
(2) cardiovascular recovery deficits. Neuromuscular efficiency
refers to the “how” of performance, specifically the degree to
which a task is performed using a minimal amount of muscle
activation. Optimal efficiency occurs when only those muscles
necessary for task completion are used, with appropriate timing
and coordination across muscles.19,34 Inefficiency, involving the
recruitment of more muscles than needed for task performance
or “incorrect pattern” of muscle activation, will lead to greater
energy demands for task performance. On the other hand, car-
diovascular recovery following physical activity refers to the extent
and the time course within which physiological functions return
to the baseline homeostatic state. This recovery is generally en-
hanced in aerobically trained individuals.35 Specifically, aerobic
(endurance exercise) training is associated with a rapid regula-
tion of postexercise metabolism and the recovery to
homeostasis.35–37 In addition, training can also improve deliv-
ery of oxygen to the active tissues, thus a reduction in the “lag”
in aerobic resources at activity onset, which subsequently impacts
the magnitude of postexercise recovery.
Appreciation of these two possible mechanisms in fatigue is
enhanced by understanding of oxygen uptake kinetics and re-
covery kinetics. The dynamic behavior of oxygen uptake in the
transition from rest to exercise is termed oxygen kinetics and
is dependent on both central circulation (i.e., delivery of oxygen
to working muscles) and peripheral extraction (i.e., ability of
working muscles to use the available oxygen). Two further rel-
evant concepts have to do with (1) oxygen deficit and (2) excess
postexercise oxygen consumption (EPOC).38,39 At the onset of
any task, anaerobic resources in the muscle are broken down until
aerobic resources come into play, observed as an achievement
of steady state in oxygen consumption to meet task demands
(Figure 1). The state that precedes the achievement of oxygen
steady state, when there is a lag in the rate of oxygen consump-
tion (i.e., inadequate oxygen supply) relative to task demands,
is termed the state of oxygen deficit.33,40 This deficit is greater
in aerobically untrained individuals than in aerobically fit indi-
viduals, in part because untrained individuals do not have efficient
oxygen delivery and extraction to meet task demands.36 In turn,
greater oxygen deficit is correlated with the increased reliance
on anaerobic resources for task performance. Anaerobic re-
sources are by nature limited and thus may be a factor in fatigue,
understood as a decline in the ability to sustain an activity. Ad-
ditionally, and related to our previous discussion of neuromuscular
efficiency, the activation of muscles irrelevant to task perfor-
mance, or activation of muscles at a level that exceeds task
demands, may further contribute to fatigue. The slower oxygen
uptake at the onset of task delays the achievement of oxygen
steady state, in turn contributing to an early onset of fatigue.41–43
This partial or total dependence on anaerobic resources
378.e3
FIGURE 1. Oxygen uptake response at the onset of exercise.
continues until either adequate oxygen is supplied to meet the
demand or fatigue prevents continued performance.17,22
The oxygen deficit incurred owing to inadequate oxygen supply
during activity leads to an oxygen debt to be “paid back” at the
cessation of activity. EPOC following physical activity refers to
the energy derived from aerobic metabolism (i.e., with oxygen)
required to replenish the anaerobic resources that have been de-
pleted during activity. EPOC represents oxygen consumed post
exercise in this process.38,39 The magnitude of EPOC is approx-
imately equivalent to the oxygen deficit incurred during the task,
when aerobic resources were insufficient.33,40 Reliance on an-
aerobic resources to meet task demands during task performance
will result in prolonged post-task recovery. Enhanced aerobic
conditioning influences recovery by increasing the delivery of
oxygenated blood to the active tissues, in turn aiding in the re-
plenishment of depleted anaerobic substrates and other
physiological processes, including decreasing heart rate and ven-
tilation, and decreasing elevated body temperature to pre-
activity levels.37
In sum, oxygen uptake plays a significant role both during
and after task performance. In the exercise physiology litera-
ture, gas exchange analysis has been used to understand oxygen
uptake and determine metabolic cost (ie, energy cost of a task)
and recovery (ie, time taken to return to baseline respiration) from
activity, to provide information about mechanisms involved in
both neuromuscular inefficiency and cardiovascular recovery
issues in fatigue.42,43
Our aim was to extend these findings from the exercise phys-
iology literature to the case of vocal fatigue, to explore possible
parallels. Specifically, our aim was to ask whether individuals
with vocal fatigue might display signs of neuromuscular inef-
ficiency implied by increased oxygen use during vocal task
performance (possibly pointing to increased muscles recruited,
or increased activation and poor timing of muscle recruit-
ment), whether they might display poor regulation of postexercise
metabolism, or both. To our knowledge, this study is the first
of its kind to use this approach in examining energy demands
of task performance to the study of vocal fatigue. The voice lit-
erature suggests that one approach to treatment of vocal fatigue
Journal of Voice, Vol. 31, No. 3, 2017
centers on voice therapy to reduce vocal hyperfunction, imply-
ing that neuromuscular inefficiency may be the base cause of
vocal fatigue.2,15,16 However, an interesting hypothesis can be en-
tertained that at least in some cases, fatigue may be as much a
problem of cardiovascular recovery as it is a problem of neu-
romuscular inefficiency. We address our questions using gas
exchange analysis.
Specific aims were to (1) determine gross metabolic cost during
vocal task performance, (2) evaluate metabolic recovery time fol-
lowing vocal task performance, and (3) explore oxygen uptake
and recovery (EPOC) kinetics in individuals with vocal fatigue
compared to individuals without vocal fatigue in two non-
fatigue groups. Hypotheses were that individuals with vocal
fatigue would (1) display increased metabolic cost during vocal
task performance, (2) display increased metabolic recovery time,
or (3) display both, compared to vocally healthy individuals
without vocal fatigue and cardiovascularly trained individuals,
the latter of which might show good post-task recovery in
particular.
METHODS
Participants
Thirty-four women between the ages of 18 and 45 years served
as participants. Participants were recruited using Institutional
Review Board–approved advertisements distributed across uni-
versity settings, public school settings, and the community at
large. Participants were allocated to one of three groups, based
on their presenting characteristics: (1) individuals with com-
plaints of vocal fatigue, with varying levels of voice training,
but no particular cardiovascular conditioning (vocal fatigue group
[VF] N = 12); (2) vocally healthy, vocally untrained,
cardiovascularly unconditioned individuals (vocally healthy group
[VH] N = 12); and (3) vocally healthy, vocally untrained,
cardiovascularly trained individuals (cardiovascular trained group
[CV] N = 10). Criteria for vocal fatigue, vocal training, and car-
diovascular conditioning were as follows. Participants were
identified as having vocal fatigue based on their scores of Vocal
Fatigue Index ([VFI] ≥24 on factor 1).44 Participants were
considered vocally healthy if VFI scores were ≤5 on factor 1
(vocally healthy and cardiovascularly trained groups). Partici-
pants were considered vocally trained if they indicated use of
voice as a professional singer or actor in the past 5 years. This
finding occurred spontaneously in the VF group and in one par-
ticipant in the VH group. Participants were considered
cardiovascularly conditioned if they reported exercising 40–60
minutes daily for at least 5 days per week and should have done
so consistently in the past 6 months, with few if any excep-
tions (American College of Sports Medicine guidelines in Refs.
29, 33). Participants were considered not cardiovascularly trained,
or sedentary, if they reported performing aerobic exercise <20–
30 minutes a day less than 3 days a week over the preceding 6
months. Sedentary versus cardiovascularly fit individuals were
recruited as part of the study to assess the role of cardiovascu-
lar conditioning on vocal task management and recovery from
the task. Females were recruited because they tend to experi-
ence vocal fatigue symptoms more often than men.45,46
Chayadevie Nanjundeswaran, et al Vocal Fatigue
TABLE 2.
Participant Demographics and Inclusionary Characteristics
Vocal Training (>5
VFI Score Years of Professional
Group (Factor 1) Experience)
VF (N = 12) ≥24 2—singing teachers
4—vocal music majors
VH (N = 12) ≤5 1—vocal music major
CV (N = 10) ≤5 0 40–60 min/d for 5 times/wk
All participants completed an online survey using Google Docs
to screen for these and other inclusionary and exclusionary cri-
teria (https://docs.google.com/spreadsheet/viewform?formkey
=dE44bXEyYjR0Z3RGX2JZNTZqM0J fMkE6MQ). General cri-
teria for inclusion across all three groups were the following:
(1) female between the ages of 18 and 45 years (the upper limit
of 45 years was chosen to restrict recruitment of women to a
relatively stable hormonal age range); (2) no known degenera-
tive or other medical conditions that would affect voice, with
the exception of seasonal allergies, asthma, or laryngopharyn-
geal reflux and their treatments; (3) self-report of competent
reading fluency in English; and (4) self-report of completion of
high school education. Table 2 provides a summary of partici-
pant demographics and inclusion criteria.
Exclusionary criteria included any evidence of (1) acute or
chronic respiratory infection at the time of testing, (2) active symp-
tomatic allergies, or (3) asthma at the time of testing, and (4)
tobacco use within the past 3 months. Additional exclusionary
criteria included (1) any history of cardiac, pulmonary, or neu-
rologic problems; (2) history of systemic diseases known to affect
voice; or (3) use of any medications known to affect voice or
oxygen uptake in the week before the experimental session.
Experimental procedures
Participants whose Google Docs were consistent with prelim-
inary inclusion and exclusion criteria were scheduled for an in-
office screening, during which they completed the Institutional
Review Board–approved informed consent. Participants with any
visible lesions or poor mobility of the vocal folds or inade-
quate glottal closure during a laryngeal examination were
excluded. The actual experimental protocol was completed on
a different day, within a week from the in-office screening.
On the day of the experimental protocol, participants were pro-
vided a verbal overview of the protocol, including (1) reading
tasks that would be used for later gas exchange analysis, fol-
lowed by (2) a consonant-vowel production task that would be
FIGURE 2. Experimental procedures.
378.e4
Cardiovascular
Fitness Mean Age, SD
6—sedentary 32.7 (9.73)
6—<20–30 min of exercise < 3 times/wk
<20–30 min of exercise <3 times/wk 26.3 (5.64)
22.9 (3.27)
later used for calculation of vocal efficiency, and finally (3) a
Bench Stepping Test that would be used to extract measures of
cardiovascular fitness. Details are as follows.
Reading tasks
A mask was placed around a participant’s nose and mouth, and
participants’ comfort with the mask was assured. A micro-
phone, part of the Lee Silverman Voice Treatment Companion
Software, was positioned at an angle of 45 degrees from the corner
of the mouth, at a distance of 30 cm as measured with a mea-
suring tape. The companion software provides ongoing measures
of loudness levels during vocal tasks. In the present study, the
software was used to measure, establish, and maintain loud-
ness levels that would be used for two different reading conditions
in the protocol: conversational (spontaneous and specific to each
participant during counting and brief conversation) and loud (10–
15 dB greater than conversational) reading conditions. Figure 2
provides an overview of the tasks for the gas exchange protocol.
During reading tasks, gas exchange data were obtained using
a portable metabolic measurement system, the MedGraphics
VO2000 (Minneapolis, MN) system. Expired gases were cap-
tured throughout the protocol, as participants breathed in through
the nose and out through the mouth. Participant demographics
including age, gender, height, and weight were obtained in the
system to adjust for metabolic measures. Baseline values were
identified as values occurring when steady-state oxygen con-
sumption level occurred for approximately 1 minute (i.e., until
variation in oxygen consumption was <0.2 mL/kg/min), before
reading tasks commenced. Reading tasks, including conversa-
tional and loud reading of junior high school level passages, were
counterbalanced across participants and commenced once base-
line was achieved. Each reading task then lasted 5 minutes to
allow time for participants to presumably reach steady-state
oxygen consumption levels in each condition.33,40,45 This study
protocol did not use tasks intended to specifically induce vocal
loading or vocal fatigue. The aim of the protocol was rather to
378.e5
explore possible metabolic responses to fairly “normal” speaking
tasks across subject groups, including those who scored poorly
on the VFI compared with those who did not.
During each vocal reading task, the LSVT Companion Soft-
ware was used to monitor speech intensity so participants would
maintain subject-specific intensity levels for comfortable and loud
speech reading. The principal investigator provided verbal feed-
back to participants, encouraging them to increase or decrease
loudness according to individually established targets through-
out the reading tasks. Following completion of each vocal reading
task, participants were provided time to rest and recover until
a 30-second recovery plateau was achieved in oxygen consump-
tion. Recovery was considered to occur when oxygen consumption
levels returned to baseline values of oxygen consumption
(<0.2 mL/kg/min) for 30 seconds.
After completion of the entire protocol, including recovery
periods, participants were asked to circle appropriate level of per-
ceived effort for each reading task retrospectively, using the Borg
Scale of perceived exertion. On this scale, values range from 6
to 20, with 6 being no exertion at all to 20 being maximal exertion.47
Metabolic costs for reading were derived from estimates of
oxygen consumption during reading. Metabolic cost is defined
as the amount of oxygen consumed standardized to task rate.
Standardization is used to account for the “workload,” for
example, to control for the rate of work in task performance.
Metabolic or energy cost of performance has been a common
measure used to investigate walking (e.g., rate of oxygen con-
sumed standardized by walking speed). Standardized by workload,
this ratio can be compared across people regardless of task rate.33,42
We applied this similar formula to assess the metabolic cost of
reading. Gross metabolic cost was standardized to the rate of
speech, in words per minute (wpm), for each participant. Thus,
metabolic cost of speech (mL/kg-w) was defined as the ratio of
energy expenditure for reading (mL/kg/min)/rate of speech (wpm).
In turn, energy expenditure for the task was calculated as average
rate of oxygen consumption from the end of the task to 1 minute
after task completion. This interval was chosen for two reasons.
First, oxygen consumption is captured from expired gases. Limited
expirations occurred during actual reading in some partici-
pants, and thus a limited number of breaths were captured for
expired gas analysis during the reading task. Second, histori-
cally, the rate of oxygen consumption during the immediate post-
task time (1 minute in this study) has been considered an
indication of the metabolic cost for the task just completed.33,48
Recovery time was calculated as time (seconds) taken to reach
baseline oxygen consumption values (within 0.2 mL/kg/min) for
30 seconds post task. This value was calculated starting 1 minute
after measures for energy expenditure for the vocal task had been
captured.
In addition to measures of metabolic cost and recovery, each
individual participant’s raw data of oxygen consumption (mL/
kg/min) were visually inspected descriptively to gain insight into
(1) pattern of oxygen use during reading, defined as oxygen uptake
kinetics and (2) recovery from reading defined as recovery ki-
netics (EPOC), as a function of group. Specifically, oxygen uptake
kinetics were inspected for the pattern in rise of oxygen con-
sumption following task onset and achievement of plateau during
Journal of Voice, Vol. 31, No. 3, 2017
the reading task. Additionally, post-reading task data were in-
spected to evaluate patterns of increase, decrease, or no change
in oxygen consumption (EPOC) post task.
Vocal efficiency task
Following completion of the reading and recovery tasks, the mask
used for collection of metabolic data was removed, and another
face mask connected to the Phonatory Aerodynamic System
(Model 6600, KayPENTAX, Montvale, NJ) was placed over the
participant’s nose and mouth. A tight seal of mask to face was
confirmed, and participants then produced three repetitions of
a five-syllable consonant-vowel string (/pi pi pi pi pi/) at com-
fortable pitch and loudness. 49 Vocal efficiency (dB SPL/
cmH20 × L/s) was later calculated for this task using values for
average estimate subglottal pressure, airflow, and speech inten-
sity across all three strings.50,51 Average estimated pressure was
obtained from average pressure peaks for the middle three tokens
of each of three five-syllable consonant vowel sets (ie, average
of peaks 2–3, 3–4, 4–5), manually selected. Pressure peaks were
evaluated for return to baseline during each vowel production,
and airflow values return to baseline during consonant produc-
tion to confirm validity of the measure.49 Flow and intensity
measures were obtained automatically by the Phonatory Aero-
dynamic System for the selected syllables.
Bench Stepping Test
The Bench Stepping Test was performed following completion
of the vocal efficiency protocol. For this test, participants were
asked to step up onto and down from a 12-inch bench for
3 minutes at 96 beats per minute as indicated by an online met-
ronome (https://www.metronomeonline.com/). Following this
stepping procedure, heart rate was manually captured for 1 minute
post exercise to provide an indication of cardiovascular fitness.
Results from the Bench Stepping Test have been widely used
to estimate cardiovascular fitness and are a good correlate of in-
strumented measures of VO2 max.52,53 This task was not used
to physically fatigue participants but rather to obtain estimates
of cardiovascular fitness.
Data analysis
To evaluate the two primary variables of interest in this study,
gross metabolic cost for reading and recovery time from reading,
inferential statistics were performed using a 2 × 3 mixed-
model analysis of variance, to evaluate metabolic cost of reading
and to evaluate recovery time. For the analysis of variance, the
within-subjects variable was task (2; conversational versus loud
reading) and the between-subjects variable was group (3; VF
versus VH versus CV). Pearson product moment correlations
were further calculated to identify possible relations between (1)
ratings of perceived exertion and metabolic cost, (2) vocal ef-
ficiency and metabolic cost, and (3) cardiovascular fitness level
and recovery time. Descriptive evaluation of the data used line
graphs to explore patterns of oxygen uptake as a function of group.
Further descriptive analyses involved obtaining the number and
percent of individuals in each group, with rise in oxygen con-
sumption (mL/kg/min) post reading (EPOC).
Chayadevie Nanjundeswaran, et al Vocal Fatigue
RESULTS
Metabolic cost of and recovery from reading
Regarding metabolic costs, collapsing values across loudness
levels, we saw no clear group differences, although numerical-
ly the CV group displayed somewhat higher values than did the
VF and the VH groups (F [2,31] = 2.308, P > 0.05, nonsignifi-
cant) (Figure 3). Collapsing values across groups, we found raw
data clearly imply greater metabolic cost for loud than for con-
versational reading, and indeed, the main effect of reading task
was significant (F [1,31] = 44.296, P < 0.001). No group × task
interaction was found (F [2,31] = 1.247, P > 0.05).
Regarding recovery times, descriptively, the VH group showed
longer mean recovery times and greater variability in recovery
times for conversational reading than did the other two groups.
The VF group had the longest recovery time for loud reading
(Figure 4). Participants in the CV group had the shortest recov-
FIGURE 3. Metabolic cost across the three groups, with vocal fatigue, vocally healthy, and cardiovascularly trained, collapsed across loudness
conditions.
FIGURE 4. Average and variability of recovery time (seconds) for conversational and loud reading across the three groups: with vocal fatigue,
vocally healthy, and cardiovascularly trained.
378.e6
ery time and least variability for both reading tasks. However,
statistically, the main effect of group was nonsignificant (F
[2,31] = .810, P > 0.05). Descriptively, recovery times were longer
for loud reading than for conversational reading tasks across all
three groups. Statistically, the main effect of task was signifi-
cant (F [1,31] = 11.408, P < 0.005), although the interaction of
group × task was not (F [2,31] = .668, P > 0.05).
Oxygen uptake kinetics
Line graphs displaying oxygen uptake kinetics were derived from
gas exchange signals captured on expiration during conversation-
al and loud reading. Representative and meaningful data are shown
in Figures 5–8. Participants in the VF group exhibited two dif-
ferent patterns of oxygen uptake kinetics: (1) a continuous rise in
oxygen uptake from the onset of the reading task to the end of the
reading task (Figure 5) and (2) no change in oxygen uptake from
378.e7 Journal of Voice, Vol. 31, No. 3, 2017

FIGURE 5. Pattern 1 of oxygen uptake kinetics in vocal fatigue, indicating a consistent rise starting at 12.27 and no plateau achieved.

baseline to the end of the reading task (Figure 6). In contrast, all
subjects in the CV group showed a consistent pattern of rise in
oxygen uptake from task onset, reaching a plateau within 2–3
minutes (Figure 7). Participants in the VH group showed three
different patterns: (1) attainment of plateau in oxygen uptake within
2–3 minutes of task onset, similar to the pattern in the CV group;
(2) continuous rise in oxygen uptake from the onset to the end of
the reading task, similar to the pattern in the VF group; and (3) a
double rise time and a double plateau, unique to this group (Figure 8).
Excess postexercise oxygen consumption
Post-reading oxygen consumption data (EPOC) were exam-
ined for a potential rise as a function of group. Descriptive data
indicating the number and percentage of individuals showing an
increase in oxygen consumption (>0.2 mL/kg/min) post reading
for each group are shown in Table 3. In brief, a greater percent-
age of participants (67%–75%) in the VF and the VH groups
showed an increase in postexercise oxygen consumption com-
pared with the CV group (37%) for both reading tasks.

FIGURE 6. Pattern 2 of oxygen uptake kinetics in six individuals with vocal fatigue, indicating no change in oxygen consumption from onset
to completion.

FIGURE 7. Oxygen uptake line graph in cardiovascularly trained individuals with rise time at 10.55 at the onset of reading and plateau achieved
at 12.17.
Chayadevie Nanjundeswaran, et al Vocal Fatigue
FIGURE 8. Line graph demonstrating atypical oxygen kinetics indicating a double plateau in a vocally healthy individual (VH8). The first rise
time is at 2.02 at the onset of reading and first plateau was achieved at 3.03, followed by a second rise time at 4.43 during the task and second
plateau was achieved at 5.43.
TABLE 3.
Number (Percent) of Individuals With a Rise in Oxygen Consumption (mL/kg/min) Post Reading (EPOC) Across the Three
Groups
With Vocal Fatigue
Task or Group n = 12
Conversational reading (n,%) 8 (67)
Loud reading (n, %) 9 (75)
Perceived phonatory effort (RPE)
Averaged ratings of perceived exertion were the greatest for the
VF group for both conversational (9.1) and loud (15.6) reading
tasks and the smallest for the CV group (conversional RPE: 6.9
and loud RPE: 11.6). The Pearson correlation between meta-
bolic cost and perceived effort for conversational loudness was
r = .044 (P > 0.05), collapsed across the three groups. The cor-
relation between metabolic cost and perceived effort for loud
reading was numerically negative but similarly insignificant
(r = −.126; P > 0.05), pooling across groups.
Vocal efficiency and cardiovascular fitness
Of the 34 participants in total, data from three participants (one
from the VH group and two from the CV group) were not avail-
able for analysis because of technical glitches and loss of collected
data. Additionally, one individual in the VF group had an un-
usually large efficiency value (443 dB/cmH20 × L/s compared
with the VF group mean average of 123.59 dB/cmH20 × L/s),
and this data point was considered an outlier and was removed
before calculating the correlation between metabolic cost and
vocal efficiency. For the remaining data, correlations between
vocal efficiency and metabolic cost for both loudness levels were
poor (r = .16, P > 0.05 and r = −.27 P > 0.05 respectively).
Similarly, poor correlations were found between indicators of
cardiovascular fitness as derived from the Bench Stepping Test
and post-reading recovery times, for both loudness tasks (r = .01,
P > 0.05; r = .14, P > 0.05 respectively).
DISCUSSION
The purpose of the study was to identify potential mechanisms
underlying vocal fatigue, specifically pertaining to (1) neuro-
muscular inefficiency and (2) cardiovascular recovery issues.
Extrapolated from the exercise physiology literature, a novel ap-
378.e8
Vocally Healthy Cardiovascularly Trained
n = 12 n = 10
8 (67) 3 (37)
6 (67) 3 (37)
proach to vocal fatigue—gas exchange analysis—was used to
explore the energy demands of vocal task performance.
In contrast to expectations, no statistically significant group dif-
ferences were noted in metabolic cost for vocal performance or
recovery time from it. However, numerically and somewhat par-
adoxically, the CV group demonstrated greater metabolic cost for
both conversational and loud reading tasks compared with the VF
and the VH groups, an observation not anticipated and indeed
counterintuitive. Additionally, the CV group had the shortest re-
covery times and the least variability in recovery times for the loud
reading task, an anticipated finding. Although the primary vari-
ables did not show results as hypothesized, secondary variables
including oxygen uptake kinetics, EPOC, and perceived phona-
tory effort provide some initial insight into potential physiological
mechanisms in vocal fatigue and protection from it. Possible ex-
planation of insignificant group differences in the pattern of
metabolic cost may be derived from the descriptive data on oxygen
uptake kinetics.
Specifically, as previously noted, oxygen uptake kinetics refer
to the dynamic behavior of oxygen uptake in the transition from
rest to exercise and provides insight into (1) availability of energy
resources to the working muscles and (2) extraction of the avail-
able energy resources by the working muscles to meet the
demands of a task. The patterns seen in all participants in the
VF group and some participants in the VH group, which in-
volved either a persistent rise or no change in oxygen uptake
during task performance, were strikingly different from the pat-
terns seen in all the CV participants, which involved a rapid rise
and plateau of oxygen consumption within 2–3 minutes of task
onset. Apparently, participants in the CV group met the demands
of the vocal task with oxygen supply (i.e., aerobic resources)
during task performance, as evidenced by their achievement of
a steady state in oxygen consumption within 2–3 minutes of task
378.e9
onset.52 On the other hand, among participants with VF, no change
or a consistent rise in oxygen uptake observed during task per-
formance may indicate a relatively greater reliance on anaerobic
energy resources for reading and a lag in oxygen supply in task
performance.41 This apparent greater reliance on anaerobic re-
sources at the onset of exercise results in a greater oxygen deficit–
or depletion of local energy stores in active tissues and must be
restored post exercise to return tissues to their pre-exercise state.
Additionally, participants in the VF group continued to rely on
anaerobic resources during task performance to meet the demands
of the task, seen as lack of achievement of steady state in oxygen
consumption. Thus, the participants with VF never attained the
state of “pay-as-you-go” of oxygen supply, matching the current
demand for energy use. Anaerobic resources are limited and may
be a factor in the development of fatigue.43,54
Evidence for such reliance on differential resources across subject
groups in this study is also supported by results of perceived pho-
natory effort ratings. Participants in the CV group reported the
least perceived effort for task completion across groups despite
the greater metabolic cost for these participants. In contrast, the
VF group reported greater phonatory effort but lower metabolic
cost numerically, compared with the CV group. Clearly, partici-
pants in the CV group were able to meet the demands of the vocal
task with oxygen supply during task performance, in contrast to
subjects in the VF and the VH groups, who did not. In other words,
participants in the CV group appeared to use an aerobic “pay-
as-you-go” approach during task performance, and experienced
less effort during the task performance, potentially because of re-
liance on aerobic as opposed to anaerobic resources. In contrast,
individuals in the VF group appear to incur oxygen deficit during
task performance owing to reliance on anaerobic mechanisms for
energy, associated with a depletion of muscle creatine phosphate
and glycogen and increased accumulation of creatine and inor-
ganic phosphates (accumulated metabolites, Table 1), thereby the
increase in perceived phonatory effort during task performance30,55
and greater oxygen debt to be paid back during recovery.
This partial or complete reliance on anaerobic metabolism for
energy demands of the task, and the lack of attainment of steady
state precludes the usual measurement of metabolic cost of per-
formance during the task. Only at steady state is the oxygen
consumed a direct reflection of the energy used. The lack of
achievement of steady state resulted in the inability to compare
and detect differences in the metabolic cost of the voice tasks across
groups. However, evidence from descriptive EPOC data in this
study indicates greater post-task oxygen consumption (ie, oxygen
required to restore local energy stores to pre-exercise state) in both
the VF and the VH groups in comparison with the CV group, a
further indication of the reliance on anaerobic resources during
task performance. Postexercise recovery is defined as the period
during which the body returns to its baseline physiological ho-
meostatic state. If oxygen deficit is incurred during task
performance, a greater need to “pay back” depleted resources will
ensue. Aerobic training can both reduce the oxygen deficit and
enhance the rate of replenishment of depleted resources due to
enhanced circulatory response as observed in the CV group.35,36
The descriptive findings suggest preliminary proposals around
potential physiological processes underlying vocal fatigue. Slower
Journal of Voice, Vol. 31, No. 3, 2017
oxygen uptake kinetics at task onset with failure to achieve a
steady state in oxygen consumption in the VF group may be at-
tributed to utilization of anaerobic resources to meet task demands.
To our knowledge, this study is the first to suggest potential re-
liance on anaerobic resources for vocal task performance and
its role in vocal fatigue. Utilization of local anaerobic re-
sources may point to poor oxygen extraction on the part of used
muscles in general, or the utilization of “wrong” combination
of muscle patterns to achieve a vocal task. Poor oxygen utili-
zation may be attributable to several mechanisms that could create
both a demand greater than the supply of oxygen and a disrup-
tion of the supply of oxygen relative to the demand, such as (1)
possible co-contraction of agonist and antagonist muscle groups,
(2) increased neuromotor recruitment of more muscles than
needed for task completion (hyperadduction) or inefficient order
of muscle recruitment, (3) decreased blood flow through the cap-
illaries due to increased constriction of the working muscles, or
(4) muscle membrane (myofascial) damage. As noted earlier, ac-
tivation of muscles at a level that exceeds task demands or
activation of muscles irrelevant to the task defines neuromus-
cular inefficiency and contributes to muscle fatigue and perceived
sensation of fatigue.41 Greater EPOC and longer recovery times
point to cardiovascular recovery issues in the VF and the VH
groups compared with the CV group.37
In sum, preliminary data suggest that the VF and the VH groups
seemed to exhibit neuromuscular inefficiency as evidenced by
potential reliance on anaerobic resources possibly attributable
to poor oxygen utilization, secondary to possible greater demand
and/or disrupted supply to the active tissues during task perfor-
mance. Additionally, the increased EPOC and poor recovery in
the VF and the VH groups indicate increased oxygen debt (ie,
depleted local tissue energy resources) to be paid back and the
additional impact of cardiovascular recovery issues. In con-
trast, data from the CV group indicated utilization of a “pay-
as-you-go” approach and rapid recovery, which are both
influenced by aerobic conditioning.35 The pattern of oxygen con-
sumption for the voice tasks and recovery in the CV group may
additionally suggest the potential influence of aerobic condi-
tioning in protection from vocal fatigue.
LIMITATIONS AND CONCLUSIONS
Although the present study revealed some interesting findings
relative to potential physiological processes in vocal fatigue, the
study is not without limitations. Although oxygen uptake kinet-
ics and EPOC patterns differentiated the CV group from the VF
group, these variables failed to differentiate the VF group from
the VH group. This outcome can be attributed to recruitment
methods and subject characteristics. All subjects including the
VF participants were recruited using community flyers and were
not self-referred to a clinic for their complaints. Recruitment of
the VF participants from a clinic may differentiate the VF group
from the VH group in future studies. There were also partici-
pant age and occupational demographic differences across the
VF and the VH groups. Participants in the VF group were all
professional voice users including teachers and performing voice
majors, whereas participants in the VH group were primarily un-
dergraduate or graduate students who did not encounter heavy
Chayadevie Nanjundeswaran, et al Vocal Fatigue
voice use on a daily basis. The recruitment of participants with
similar vocal demands and demographics but with differences
in VFI scores for the VF and the VH groups might help differ-
entiate the metabolic profiles between these groups in the
future.
Additionally, the oxygen consumption recorded during and
after the vocal reading task was a global measure of physiolog-
ical energy expenditure during task performance and task recovery,
reflecting metabolic activity across all subsystems involved in
voice production including laryngeal, respiratory, articulatory,
and central nervous system activity. Future research protocols
will need to distinguish specific involvement of these different
systems and their contributions to vocal fatigue, in particular
central versus peripheral contributions. Additionally, future pro-
tocols will need to identify potential outcome measures to capture
anaerobic mechanisms during vocal task performance.
Although the study has some limitations, the data do provide
potential preliminary insight into oxygen uptake and recovery
kinetics and their possible role in mechanisms of vocal fatigue.
Hopefully, these insights may lay the foundation for future
research.
Acknowledgment
This research was completed as part of the requirements of a
doctoral dissertation. The authors would like to acknowledge the
SHRS research development fund and the ETSU Foundation grant
that was critical in recruiting participants for the study.
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