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European Archives of Oto-Rhino-Laryngology (2021) 278:159–165

https://doi.org/10.1007/s00405-020-06238-7

LARYNGOLOGY

Vocal resistance among choir singers


Fernanda Onofre1 · Hilton Ricz1 · Yuka de Almeida Prado2 · Gleidy Vannesa E. Rojas1 · Denny Marcos Garcia1 ·
Lilian Aguiar‑Ricz1

Received: 23 April 2020 / Accepted: 22 July 2020 / Published online: 4 August 2020
© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract
Purpose The purpose of the present study was to compare the voice of choir singers before and after 60 min of singing and
after an absolute rest.
Methods Twenty-one female choir singers aged on average 26.59 years, with experience in choir singing of at least one
year were instructed to emit the vowel /a/ before and after singing and after a vocal rest of 30 min for an analysis of acoustic
measures, and for the evaluation of their tactile–kinesthetic self-perception. Vocal warm-up was performed for 10 min. The
participants were instructed to sing the “Ave Verum” music continuously for 60 min.
Results f0 (p = 0.0001) and Flo (p = 0.0002) increased after the singing test and were reduced after the vocal rest, in con-
trast to Fhi (p = 0.001), which continued to be increased compared to the pre-test measure even after the vocal rest. The
vAm parameter (p = 0.05) was reduced after continuous singing and rest. All self-evaluation symptoms increased after the
continuous singing task and were reduced after the 30 min rest, except for complaints of low voice, pain when swallowing
and cough/throat clearing.
Conclusion 60 min of continuous use of the singing voice induced signs of vocal fatigue with an increase in f0, with improve-
ment of symptoms and a reduction of f0 occurring after 30 min of vocal rest.

Keywords Vocal loading · Vocal loading task · Voice health · Voice resistance · Vocal fatigue

Introduction Vocal complaints are frequent after singing, even with


vocal warm-up [3], especially among more experienced
An excessive vocal demand has negative effects on a variety singers who usually report more symptoms after a perfor-
of professions, with the occurrence of fatigue of the vocal mance by paying more attention to throat sensations and
cord muscles and heavy vocal loading [1]. Singers are pro- to vocal quality [4]. This also applies to those who study
fessionals who depend on the quality of their voice for their the voice since they have reasonable knowledge and aware-
performance. Thus, to preserve their voice and prepare it ness of perception and more preoccupation about their vocal
for singing activity, they have adopted techniques of vocal health [5].
warm-up and cool-down for rehearsals and presentations; if Singing is still little understood regarding its mechanism
these procedures are not followed, voice professionals are at and vocal behavior in high musical performance. Heavy
risk for injuries [2]. vocal loading or effort is defined as the prolonged and con-
tinuous use of the voice and has been reported to include
four phases: warm-up (adaptation to the speaking task), per-
* Lilian Aguiar‑Ricz
formance (adaptation), fatigue (self-report of physical effort
liricz@fmrp.usp.br associated with voice changes), and recovery [6,7].
Among teachers, voice recovery occurs 4–6 h after 2 h
1
Department of Ophthalmology, Otorhinolaryngology of prolonged use of the voice, alhough full voice recovery
and Head and Neck Surgery, Ribeirão Preto Medical School,
University of São Paulo, Av. Bandeirantes, 3900. Monte
occurs only after 12–18 h [8]. A lower effort to speak can
Alegre, Ribeirão Preto, SP 14048‑900, Brazil be observed after 15 min of vocal silence [9], although the
2
Department of Music, Faculty of Philosophy, Sciences
phonation pressure threshold returns to normal only after
and Letters at Ribeirão Preto, University of São Paulo, 1 h of vocal rest [10]. Among opera singers, a vocal rest on
Ribeirão Preto, SP, Brazil

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160 European Archives of Oto-Rhino-Laryngology (2021) 278:159–165

the day after a performance may facilitate recovery [11]. discomfort and without water intake. The piece chosen was
Among choir singers, the vocal parameters are altered after the Ave Verum Corpus motet Ré3 to Mi4 by Wolfgang Ama-
60 min of singing and the fundamental frequency increases, deus Mozart (1756–1791), previously selected taking into
appearing to be the parameter that is able to characterize consideration the knowledge and the training of the choir
vocal resistance or effort [12]. singers. The performance was accompanied by a playback
However, it is not known how long it is possible to sing of 1′58 duration of the recorded music sung, being repeated
without generating vocal fatigue or how much time is suf- from the beginning to the end (“da capo al fine”) up to the
ficient to characterize vocal loading or effort for the vocal time when the singer was able to execute it, with a mean of
tract, or even what rest time is needed for the voice to return 30 repetitions. Each participant sang in the appropriate tone
to normal conditions after singing. Thus, the objective of for a soprano. After singing for up to 60 min, the singers
the present study was to compare the voice of young choir remained absolutely silent for 30 min.
singers before and after a continuous singing task lasting up For the analysis of the vocal register, the singers recorded
to 60 min, and after a 30 min rest. three prolonged emissions of the vowel /a/ in the habitual
register, intensity and vocal frequency for more than 3 s
using a unidirectional microphone at three time points:
Methods before the test (basal), after the 60 min vocal resistance
test (singing test), and after 30 min of absolute vocal rest.
Ethical considerations Acoustic analysis was carried out using the Advanced Multi-
Dimensional Voice Program (MDVP-Adv) software (Com-
The study was approved by the Research Ethics Committee puterized Speech Lab, Kay P ­ entax®). The parameters used
of the University Hspital, School of Medicine of Ribeirão are listed in Table 1.
Preto, University of São Paulo (protocol number 7716/2012), The self-perception of signs and symptoms was assessed
and all subjects gave written informed consent to participate. with a psychometric instrument consisting of a self-assess-
ment questionnaire covering tactile, kinesthetic and auditory
Sample manifestations [13,14]. The participants responded to the
questionnaire before and after the test of prolonged use of
A prospective cohort study was conducted on 21 music stu- the voice, considering the 13 following signs and symptoms:
dents, all of them soprano choir singers aged 18–39 years hoarseness, dry throat, voice breaks, sore throat, difficulty
(mean: 26.59 years) with experience of at least 1 year in in speaking, high-pitched voice, low voice, vocal fatigue,
choir singing. Exclusion criteria were: a history of dyspho- cough, and/or throat clearing. The participant was asked
nia, a previous diagnosis of gastroesophageal reflux, hormo- to quantify each item of the questionnaire using a 100 mm
nal alterations, a diagnosis of rhinitis, diseases of the res-
piratory apparatus, and hearing, neurological or psychiatric
disorders. Regarding habits, also excluded were smokers, Table 1  Acoustic parameters used for vocal evaluation
users of psychoactive substances or of continuous medica-
Acoustic measurements
tions, such as antihistamines and antidepressant, antihy- Advanced multi-dimensional voice program—MDVP Adv, Kay
pertensive, blood glucose lowering and anti-inflammatory ­Pentax®
drugs.
f0 (Hz): Average fundamental frequency
Fhi (Hz): Highest fundamental frequency
Procedures
Flo (Hz): Lowest fundamental frequency
PFR (Semi-Tones): Phonatory fundamental frequency range
A vocal resistance test was applied in the afternoon, with the
vF0 (%): Coefficient of fundamental frequency variation
singers being instructed to consume a bland diet and to have
PPQ (%): Pitch period perturbation quotient
the last meal 2 h before the test, so that gastric emptying
APQ (%): Amplitude perturbation quotient
would occur and gastroesophageal reflux would be avoided.
RAP (n): Relative average perturbation
Before the test, the participants performed a previously
Fftr (Hz): f0-Tremor frequency
standardized vocal warm-up of 10 min by singing the vowel
Fatr (Hz): Amplitude-tremor frequency
habitually used by each singer to exercise vocalization, with
FTRI (%): Frequency tremor intensity index
the voice rising and falling a semitone of a vocally com-
NHR (n): Noise-to-harmonic ratio
fortable note, from the lowest to the highest, while being
vAm (n): Peak amplitude variation;
accompanied by a singing teacher using the sound of a
VTI (n): Voice turbulence index
keyboard. The participants were instructed to sing continu-
SPI (n): Soft phonation index
ously for 60 min, with respiratory pauses to avoid any vocal

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European Archives of Oto-Rhino-Laryngology (2021) 278:159–165 161

visual analogue scale, where 0 indicated absence and 100 It is generally accepted that variables that influence the
indicated maximum. tension of normal skeletal muscles include morphological,
The 60 min vocal resistance test started after the initial biomechanical, neurological, metabolic and biochemical
recordings of the voice samples and of self-perception. The factors. For this reason, in the present study, we controlled
participant performed in an acoustically treated room (noise motor activity during the singing of the same music, as well
of less than 50 dB) with monitoring of air relative humidity as the environment, hydration and feeding, so that these fac-
(mean: 42.3%) and temperature (mean: 24.7 °C). tors would not interfere with the final response. Even people
with a normal voice report vocal fatigue in the presence
Statistical analysis of allergies or infections when the vocal folds are likely to
become inflamed [15]. Another aspect considered is the uni-
The intra- and inter-subject results of the computed acoustic formity of choir singers.
analysis and of the numerical scale for perceptive-auditory It is understood that a prolonged use of the voice may
and tactile–kinesthetic self-evaluation of the voice were lead to increased fundamental frequency, a fact that can be
compared before and after the singing test. Data are reported interpreted as a normal physiological adaptation of the vocal
as mean ± SE and were submitted to descriptive and inferen- apparatus to speech, and therefore as a sign of vocal health
tial analyses. The mean data for the three distinct times were [16].
compared by unifactorial analysis of variance with repeated An hour of prolonged use of the voice causes an increase
measures (one-way ANOVA-RM). When a significant differ- in F0, a reduction of the glottic noise, an increase in vocal
ence between means was observed, the Tukey HSD (honest pitch, loudness, projection and stability, and a reduction
significant differences) post test for multiple comparisons of the general degree of dysphonia, vocal roughness and
was applied. The analyses were carried out using the Origin breathiness, indicating that the increased tonicity of the
Pro 9.0 software (OriginLab, Northampton, MA), with the laryngeal adductor muscles for phonation and self-percep-
level of significance set at 5%. tion reveals a phonatory effort [17]. The increase in f0 may
be a sign of warm-up, but may also be a marker of voice
resistance or heavy loading.
After 60 min of singing, the fundamental frequency of
Results the choir singers increased. This increase is an alert signal
regarding the importance of a situation of vocal fatigue and
The acoustic vocal parameters obtained from the analysis may not simply be a condition of muscular warm-up. Among
of the sustained emission of the vowel /a/, modal record- voice professionals, frequency breaks followed by hoarse-
ing, before the vocal resistance test (basal), after the 60 min ness are observed after vocal abuse or after a prolonged use
test of vocal resistance (singing test) and after 30 min of of the voice, suggesting vocal loading with the excessive use
absolute vocal rest (rest) are listed in Table 2. An increase of force and contraction of layngeal muscles that signal to
in mean values was observed after the vocal singing test, the larynx that there is vocal effort and resistance [18]. Nev-
followed by a decrease after rest for the f0 (p = 0.0001) and ertheless, it seems that the vibratory capacity of the vocal
Flo (p = 0.0002) parameters. An increase in mean results folds is maintained even after the prolonged use of the sing-
occurred after the vocal resistance test and after rest for Fhi ing voice [19], and even with incomplete glottic closure,
(p = 0.001), while a decrease in mean results was observed there is no influence on the pitch and loudness of either the
for vAm (p = 0.05) at the same time points. speaking or the singing voice of young women [20].
Table 3 lists the values obtained at the pre- and post-sing- There is no consensus about whether or not the prolonged
ing time points and after rest for the analysis of questions of use of the singing voice can induce resistance to vocal
perceptive–auditory and tactile–kinesthetic self-assessment fatigue. It is not known how much time of use of the singing
of phonation. voice can impair the normal functioning condition of the
larynx, with the possible occurrence of an individual varia-
tion in vocal resistance [21]. It is necessary to take into con-
Discussion sideration the conditions, experience, profissionalism and
musical style of the singers since even trained opera singers
A wide variety of methods, as well as different samples, are exhibit changes with the continued use of the voice without
used to study vocal resistance. The proposal of the present a rest, suggesting that a vocal rest is essential [11].
study was to report the results of prolonged use of the voice However, singing is an action that requires a large amount
for 60 min by choir singers and to determine whether there of energy on the part of the singer. It should be kept in mind
are changes in vocal parameters and in self-perception of that professional singers develop a physiological adaptation
vocal signs and symptoms after an absolute rest of 30 min. of the muscles, with a consequent adaptation to excessive

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Table 2  Acoustic parameters determined before and after 1 h of singing and after a 30 min rest
Parameters Pre-singing After singing Rest p value
Mean ± standard Range Median Mean ± standard Range Median Mean ± standard Range Median
deviation deviation deviation

f0 (Hz) 227.9 ± 20.7 188.2–275.3 228.3 247.1 ± 28.3 200.4–300 239.8 245 ± 28.5 186.5–291 249 0.0001
Fhi (Hz) 238.4 ± 26 190.6–296 237.7 255 ± 29.7 203.6–306.5 250.1 257.1 ± 33.2 195.6–335.6 258.6 0.001
Flo (Hz) 218.2 ± 18.9 184.2–254.2 221.3 239.8 ± 27.7 198.1–293.3 233.8 234.3 ± 28.4 180.7–285.4 238.3 0.0002
PFR (Semi-Tones) 2.5 ± 1.26 1–5 2 2.27 ± 0.63 1–4 2 2.52 ± 1.5 1–7 2 0.65
vF0 (%) 1.08 ± 0.54 0.43–2.45 1.02 0.83 ± 0.31 0.44–1.4 0.74 1.03 ± 0.58 0.443–2.8 0.83 0.09
PPQ (%) 0.61 ± 0.41 0.14–1.54 0.53 0.43 ± 0.25 0.12–1.08 0.35 0.59 ± 0.45 0.11–2.05 0.5 0.15
APQ (%) 2.05 ± 0.82 0.86–3.72 1.82 1.92 ± 0.7 0.83–3.99 1.74 2.47 ± 2.56 1.1–13.28 1.86 0.406
RAP (n) 0.62 ± 0.42 0.14–1.49 0.57 0.44 ± 0.25 0.12–1.08 0.37 0.61 ± 0.44 0.1–1.98 0.51 0.14
Fftr (Hz) 4.09 ± 1.25 2.06–7.14 4.1 4.67 ± 1.84 2.21–9.09 4.7 4.56 ± 2.06 2.19–11.11 4.39 0.48
Fatr (Hz) 4.17 ± 1.68 2.06–7.54 4.08 3.85 ± 1.79 2.11–7.01 3 3.88 ± 1.41 2.13–6.06 3.47 0.6503
FTRI (%) 2.66 ± 2.63 0.06–9.54 2.55 1.76 ± 1.75 0.01–6.53 1.47 1.65 ± 2.03 0.13–5.73 0.31 0.09
NHR (n) 0.11 ± 0.01 0.08–0.15 0.12 0.11 ± 0.02 0.07–0.15 0.11 0.11 ± 0.01 0.07–0.139 0.11 0.47
vAm (n) 9.71 ± 4.53 4.31–20.36 8.68 8.16 ± 3.45 3.63–19.56 7.44 7.59 ± 2.79 3.7–15.27 7.2 0.05
VTI (n) 0.05 ± 0.01 0.01–0.09 0.04 0.04 ± 0.01 0.01–0.07 0.04 0.04 ± 0.01 0.01–0.05 0.04 0.18
SPI (n) 8.53 ± 4.97 4.02–21.75 7.04 9.01 ± 5.24 2.58–25.80 8.16 10.45 ± 6.02 2.13–21.52 8.46 0.3353
European Archives of Oto-Rhino-Laryngology (2021) 278:159–165
European Archives of Oto-Rhino-Laryngology (2021) 278:159–165 163

vocal loading. In the present study, after 1 h of continuous

< 0.0001
0.0002
< 0.0001
0.0004

0.005
0.007
0.007
0.033
0.002
0.005
p value
singing, the choir singers demonstrated increased tension

0.06
0.16
0.8
of the musculature, suggesting vocal warming [16,22,23].
Changes in acoustic measures, such as F0 elevation and a
reduction of perturbation of the measures, such as jitter and
Median

shimmer, indicate an increase in muscle activity (increased

0.63
0.85
1.8 tonus) in an attempt to adapt phonation [24]. Vocal warm-

0
0
0
0
0
0
0
0
0
0

up promotes the quality of the voice, and acoustic analysis


appears to be a valuable and sensitive instrument for the
Range

0–4.4
0–4.6
0–2.4
0–5.5
0–6.5
0–2.4
0–8.5
0–5.5
0–2.1
0–7.5
0–8.4

quantitation of this effect [25]. When there is an increase

0–0
0–7

in pitch, there is possibly a greater gain in muscle activ-


ity which contributes to the tension of the vocal folds [26],
Mean ± standard

since it is understood that there is the need to recruit a larger

0.65 ± 1.16
0.89 ± 1.56
0.72 ± 1.61
1.72 ± 2.28
0.38 ± 1.22
0.10 ± 0.45

number of fibers and muscles in the presence of heavy vocal

0.6 ± 0.83
0.46 ± 0.8
2.6 ± 2.57
0.8 ± 1.96
deviation

0 ± 1.53
1.07 ± 2

loading to maintain the force and tension of the vocal folds.


0±0
Rest
Table 3  Self-assessed values of signs and symptoms (0–100 visual analogue scale), before, after one hour of singing and after a 30 min rest

Although f0 seems to be the most robust parameter for the


determination of laryngeal muscle fatigue [27], it should be
pointed out that it is extremely complex to determine vocal
Median

fatigue [23]. An increase in f0 is not always demonstrated


1.05
1.65
3.15
1.75

1.8
3.5
5.4

after a test involving the continuous use of the voice [28]


0
0
0
0
2
0

and other parameters, such as RAP, APQ, SPI and vAm,


may also change [22]. A reduction of vAm was detected in
Range

0–8.2
0–8.2
0–8.4
0–7.9
0–1.4
0–6.9
0–4.1
0–7.9
0–7.9

0–10
0–10
0–10

the 21 singers studied here after continuous singing and rest.


0–4

Another parameter that was modified among the choir


singers studied was Flo, which increased after the sing-
Mean ± standard

ing test and decreased after rest. This finding permits us to


After singing

1.83 ± 2.46
2.65 ± 2.27
2.27 ± 2.74
2.01 ± 2.75
0.11 ± 0.37
1.66 ± 1.81
0.65 ± 1.32
3.61 ± 3.21
0.65 ± 1.23
2.41 ± 2.43

infer that a 30 min rest was sufficient for the recovery of the
2.21 ± 2.2
3.27 ± 2.6
5.13 ± 2.9
deviation

laryngeal adaptations that occurred during singing since the


lower fundamental frequency observed cycle by cycle in the
singers was reduced with rest and with the consequent vocal
cool-down. However, Fhi continued to be high even after the
Median

rest, revealing the difficulty in finding acoustic parameters


1.45
1.75
2.7

that are related to vocal fatigue [29].


0
0
0
0
0
0
0
0
2
0

It is difficult to compare studies due to the lack of uni-


formity regarding tests, subject gender and age. It is neces-
Range

0–7.9
0–1.4
0–3.1
0–2.1
0–3.8
0–7.1
0–1.1
0–1.5
0–8.1
0–6.8
0–5.9

sary to reflect about the results of acoustic measurements in


0–4
0–0

studies of resistance to vocal fatigue, with questions raised


about how sensitive the method really is to provide a reliable
Mean ± standard

result, or how effective these parameters are to identify cor-


Pre-singing

1.46 ± 1.89
0.68 ± 1.01
0.27 ± 0.94
0.17 ± 0.55
0.61 ± 1.15
2.04 ± 2.30
0.21 ± 0.49
2.35 ± 2.67
1.07 ± 1.66

rectly which of the individuals evaluated really show char-


0.25 ± 0.5
0.1 ± 0.31
3.1 ± 2.12
deviation

acteristics of resistance or how specifically a method is in


0±0

revealing the individuals who do not have vocal fatigue [24].


The duration of rest after an intense use of the voice
is also not clearly defined. 15 min of vocal rest may pro-
Pain/tension in shoulders and neck

mote a lower effort in speaking [9], and 1 h of rest per-


mits the phonatory pressure threshold to return to normal
Cough and throat clearing

[10]. Among the choir singers sudied here, after 30 min,


Pain when swallowing

there was a clear improvement of self-perception of signs


Difficulty in speaking
Signs or symptoms

and symptoms related to vocal production, in addition to


Effort to speak

evidence regarding the acoustic parameters. Subjects with


Vocal fatigue
Voice breaks

Weak voice
Hoarseness

Sore throat

High voice

greater vocal experience report more vocal complaints after


Low voice
Dry throat

a performance by valuing more the sensations of the throat


and the vocal quality [4].

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164 European Archives of Oto-Rhino-Laryngology (2021) 278:159–165

This finding favors the prescription of absolute vocal rest The methodology applied here to the singers provided
so that the musculature will reorganize and return to its natu- advances in the knowledge about this topic, with answers
ral state. Thus, after a vocal rest, singers can use their voice regarding the situation of vocal resistance to vocal fatigue.
again without hurting their health, with a greater longevity For the study, a low-magnitude test, repetitive and sustained
of their artistic career. However, the resistance of laryngeal for 60 min, was applied, with the evaluation not only of
tissue is one of the major aspects of vocal fatigue, with the the acoustic measures, but also of the self-perception of
curve of the trajectory of recovery being similar to that of symptoms.
the recovery from a chronic dermal wound. Thus, with the New studies of the effects of vocal resistance to fatigue
intensive daily use of the voice, the continuous damage to are needed to establish effective methods for the training of
the laryngeal mucosa causes the cure mechanisms to be in vocal resistance and the use of cool-down techniques after
a constant state of repair and, in the short term, 50% of the a musical performance, thus providing scientific evidence
recovery occurs after about 4–6 h and full recovery occurs and supporting singers in the refinement of the execution
after 12–18 h of intense use of the voice [8]. A rest before of their art.
[30] and after a performance [11] is essential for singers.
The practice of vocal cool-down is extremly important for
singers [12], although it is not commonly applied [3]. Conclusion
Complaints, or signs and symptoms are parameters that
characterize vocal fatigue [1]. It is understood that, the larger The test of continuous voice use for 60 min applied to choir
the number of vocal complaints, the higher the f0 and, the singers induced a high effort, increasing f0, Flo and Fhi,
longer the time of vocal intensity, the greater the vocal prob- demonstrating that the fundamental frequency was sucepti-
lems [31]. ble to singing uninterruptedly for 1 h. However, the increase
Among the choir singers studied here, the indications of in symptoms indicated the occurrence of vocal fatigue.
tactile–kinesthetic and auditory symptoms were obtained In addition, we observed that 30 min of rest was sufficient
with the use of a visual analogue scale, demonstrating an to attenuate the symptoms and to reduce f0.
increase in the auditory, tactile and kinesthetic perception
after the prolonged use of the voice, as also observed in pre-
vious studes of vocal resistance [4,9,10,23,24,32]. Funding None.
The present singers were asked about hoarseness to
obtain information about the tactile–kinesthetic and auditory Compliance with ethical standards
manifestations after singing and after a rest. They reported
increased hoarseness after the test and a reduction after the Conflict of interest The authors declare that they have no conflict of
interest.
rest. The complaint of hoarseness is not usually noted after
tests of resistance to vocal fatigue. The present singers prob- Ethics approval All procedures in studies involving human participants
ably have a more refined auditory sense regarding the ques- were in accordance with the ethical standards of the national research
tion of vibration of the vocal cords. committee and with the 1964 Helsinki.Declaration and its later amend-
ments. This study was approved by the Research Ethics Committee of
A dry throat is a change easily observed after the use of
the Clinics Hospital of the School of Medicine of Ribeirão Preto of
the voice [19] and the studied singers reported an increase the University of São Paulo according to protocol number 9711/2008.
in this sennsation after the vocal resistance test, with reduc-
tion after the rest. Informed consent Informed consent was obtained from all individual
participants included in the study. Participants signed informed consent
Singers who do not have the habit of resting or of using
regarding publishing their data.
vocal cool-down techniques may report perceptive voice
complaints after an intense use of the voice. In the present
study, the singers pointed out an increased perception of
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