Vocal Signs and Symptoms Related to COVID-19 and Risk Factors for their Persistence

Abstract

Objective: To compare the occurrence of vocal signs and symptoms before, during, and after coronavirus disease (COVID-19) and analyze possible risk factors for the persistence of these signs and symptoms after disease resolution.
Method: This was an observational, analytical, and cross-sectional study. The participants were 45 individuals of both sexes, with a mean age of 44 years, who were previously affected by COVID-19. All participants answered a questionnaire about sociodemographic data, smoking history, disease course, vocal complaints, and the vocal signs and symptoms list (SSL), referring to three timepoints (before, during, and after COVID-19).
Results: The most commonly reported vocal signs and symptoms before COVID-19 were phlegm (26.67%; n=12) and dry throat (24.44%; n=11). During COVID-19, the most frequent vocal signs and symptoms were tired voice after short-term use (73.33%; n=33) and dry throat (71.11%; n=32). After the disease, the most reported vocal signs and symptoms were dry throat (57.78%; n=26) and phlegm (53.33; n=24). The self-perception of vocal signs and symptoms before COVID-19 was lower than that during and after COVID-19 (p<0.001). Vocal complaints after COVID-19 and oxygen therapy were predictors of self-perception of vocal signs and symptoms after COVID-19.
Conclusion: Individuals affected by COVID-19 had a higher frequency of vocal signs and symptoms during the disease. However, after remission, the frequency of vocal signs and symptoms was higher than that at baseline. The need for oxygen therapy may indicate a risk for a higher occurrence of vocal signs and symptoms after COVID-19.

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Vocal Signs and Symptoms Related to COVID-19 and Risk
Factors for their Persistence
*,†
Ana Paula Dassie-Leite,
‡
Tatiane Prestes Gueths,
§,║
Vanessa Veis Ribeiro, *Eliane Cristina Pereira,
*Perla do Nascimento Martins, and
¶
Christiane Riedi Daniel, *yIrati, z{Guarapuava, xLagarto, and ║Jo~
ao Pessoa, Brazil
Abstract: Objective. To compare the occurrence of vocal signs and symptoms before, during, and after coro-
navirus disease (COVID-19) and analyze possible risk factors for the persistence of these signs and symptoms
after disease resolution.
Methods. This was an observational, analytical, and cross-sectional study. The participants were 45 individuals
of both sexes, with a mean age of 44 years, who were previously affected by COVID-19. All participants
answered a questionnaire about sociodemographic data, smoking history, disease course, vocal complaints, and
the vocal signs and symptoms list (SSL), referring to three timepoints (before, during, and after COVID-19).
Results. The most commonly reported vocal signs and symptoms before COVID-19 were phlegm (26.67%;
n=12) and dry throat (24.44%; n=11). During COVID-19, the most frequent vocal signs and symptoms were tired
voice after short-term use (73.33%; n=33) and dry throat (71.11%; n=32). After the disease, the most reported
vocal signs and symptoms were dry throat (57.78%; n=26) and phlegm (53.33; n=24). The self-perception of vocal
signs and symptoms before COVID-19 was lower than that during and after COVID-19 (P<0.001). Vocal com-
plaints after COVID-19 and oxygen therapy were predictors of self-perception of vocal signs and symptoms after
COVID-19.
Conclusions. Individuals affected by COVID-19 had a higher frequency of vocal signs and symptoms during
the disease. However, after remission, the frequency of vocal signs and symptoms was higher than that at base-
line. The need for oxygen therapy may indicate a risk for a higher occurrence of vocal signs and symptoms after
COVID-19.
Key Words: COVID-19−Dysphonia−Signs and symptoms−Voice.
INTRODUCTION
COVID-19 is caused by severe acute respiratory syndrome
coronavirus 2 (SARS-CoV-2). The virus has a clinical spec-
trum ranging from asymptomatic infections to deaths.
1
Approximately 80% of COVID-19 patients may be
asymptomatic or oligosymptomatic (few symptoms). Of the
20% who require hospital care because they have difficulty
breathing, approximately 5% may require oxygen therapy
due to hypoxemia.
1
Acute symptoms of COVID-19 include cough, fever, dys-
pnea, musculoskeletal symptoms (myalgia, joint pain,
fatigue), gastrointestinal symptoms, anosmia, and dysgeu-
sia.
2−4
COVID-19 can lead to respiratory complications,
which in turn may result in cardiac (arrhythmias and
myocardial), renal (acute kidney injury), gastrointestinal,
neurological (neuropathy, encephalopathy), endocrine, and
musculoskeletal consequences (weakness, pain, and
fatigue).
5,6
Despite numerous studies on the acute form of COVID-
19, to date, there is no established deadline to describe the
slow and persistent condition in individuals with long-term
sequelae of COVID-19.
7
Abnormal signs and symptoms or
parameters that persist for more than 2 weeks after the onset
of COVID-19 and do not resolve (baseline values) may have
potential long-term effects.
8
These symptoms occur mainly
in survivors of severe and critical COVID-19, and long-last-
ing effects also occur in individuals with mild infection and
those who require no hospitalization.
9
Patients who had COVID-19 and required medical hospi-
talization often have symptoms after approximately 2
months,
10,11
especially those who needed intensive care unit
(ICU) care.
11
The main symptoms are fatigue,10
,11
dyspnea,
10,11
joint pain,
10
chest pain,
10
and psychological
distress.
11
Voice-related symptoms, more specifically related
to laryngeal sensitivity and vocal changes, have also been
described.
11
Regarding vocal symptoms, a single study specifically on
this topic analyzed the prevalence of dysphonia in 702 Euro-
pean patients with mild to moderate COVID-19. The data
showed that 27% of the patients had dysphonia. Dysphonic
patients had a higher occurrence of cough, chest pain, sticky
sputum, arthralgia, diarrhea, headache, fatigue, nausea,
and vomiting. The severity of dyspnea, dysphagia, ear pain,
Accepted for publication July 21, 2021.
Funding: None.
From the *Professor at the Speech-Language Pathology Department, Universidade
Estadual do Centro-Oeste - UNICENTRO. PR 156, Km 07; Irati, Paraná, Brazil; y-
Professor at the Interdisciplinary Postgraduate Program in Community Development,
Universidade Estadual do Centro-Oeste - UNICENTRO. PR 156, Km 07; Irati, Par-
aná, Brazil; zSpeech Language Pahologist. Saldanha Marinho st, 2820. Bairro dos
Estados; Guarapuava, Paraná, Brazil; xProfessor at the Speech-Language Pathology
Department, Universidade Federal de Sergipe - UFS. Governador Marcelo Dedá
Avenue, 13, Centro, Lagarto, Sergipe, Brazil; ║Professor at the Associate Postgradu-
ate Program in Speech-Language Pathology, Universidade Federal da Paraíba -
UFPB. Cidade Universitária, Conjunto Presidente Castelo Branco III, Jo~
ao Pessoa,
Paraíba, Brazil; and the {Professor at the Physioterapy Department, Universidade
Estadual do Centro-Oeste - UNICENTRO. Alameda

Elio Antonio Dalla Vecchia,
838 - CEP 85040-167 - Bairro - Vila Carli, Guarapuava, Brazil.
Address correspondence and reprint requests to Ana Paula Dassie-Leite, Universi-
dade Estadual do Centro-Oeste - UNICENTRO, PR 156, Km 07; Irati, Paraná
84500-000, Brazil. E-mail: pauladassie@hotmail.com
Journal of Voice, Vol. &&, No. &&, pp. &&−&&
0892-1997
© 2021 The Voice Foundation. Published by Elsevier Inc. All rights reserved.
https://doi.org/10.1016/j.jvoice.2021.07.013
ARTICLE IN PRESS

facial pain, sore throat, and nasal obstruction was higher in
the dysphonic group than in the non-dysphonic group.
12
It is believed that the vocal symptoms present after
COVID-19 may not only be related to orotracheal intuba-
tion
13
but also to respiratory sequelae. In clinical practice,
vocal complaints associated with respiratory complaints
have been observed. This is because the integrity of the
respiratory system is fundamental for proper voice produc-
tion with respect to providing the air pressure necessary for
phonation.
14−17
Moreover, in the new scenario imposed by
COVID-19, some laryngeal occurrences have been
described, with scarcely known causes, as paradoxical
movement of the vocal fold.
12
It is necessary to understand more deeply the occurrence of
vocal signs and symptoms before, during, and after COVID-
19. Thus, it is possible to contribute to the management of
symptoms and maximize the functional recovery of patients.
11
Therefore, this study aimed to compare the occurrence of
vocal signs and symptoms before, during, and after coronavi-
rus disease (COVID-19) and analyze possible risk factors for
the persistence of these symptoms after disease resolution.
MATERIAL AND METHODS
This study has an observational, analytical, cross-sectional,
and hybrid design. The study was approved by the Ethics
Committee on Research with Human Beings of the institu-
tion of origin, under number 4.319.245.
Individuals referred by the health department of a Brazil-
ian municipality to the evaluation and rehabilitation service
after COVID-19 developed by the home institution partici-
pated in the study. The service is composed of speech thera-
pists and physiotherapists.
The inclusion criteria were as follows: both sexes, age
≥18 years, a diagnosis of COVID-19 confirmed by reverse
transcription polymerase chain reaction (RT-PCR), and
referral from the public health service of the city where the
institution proposing this research is located. Exclusion cri-
teria were: asymptomatic persons; invasive mechanical ven-
tilation; history of respiratory disorders or other health
changes that impacted voice and communication before
COVID. The eligibility criteria were applied using direct
questions.
All participants answered a questionnaire about sociode-
mographic data (sex, age, weight, and height), smoking
history, course of the disease (date of diagnosis, need for
hospitalization, type and duration of hospitalization, nonin-
vasive mechanical ventilation, oxygen therapy), and vocal
complaints (before, during, and after COVID-19).
Following this, the individuals answered the vocal signs
and symptoms list (SSL), which investigates the presence or
absence of 14 vocal signs or symptoms.
18
A brazilian portu-
guese translation of the instrument was used.
19
Each symp-
tom was addressed with respect to three distinct timepoints:
before, during, and after COVID-19. According to the
authors'instructions, the total score of the questionnaire
was calculated using a simple sum. Moreover, a descriptive
analysis of individual symptoms was conducted.
The vocal symptoms were self-reported based on the fol-
lowing questions: Vocal signs and symptoms before
COVID-19 - participant should answer considering whether
the sign/symptom was recurrent or persistent in his/her day-
to-day before the diagnosis of the disease; Vocal signs and
symptoms during COVID-19 - participant should respond
considering if the sign/symptom questioned occurred during
the active period of the disease, which comprised the inter-
val between the 3rd and 11th day; Vocal signs and symp-
toms after a COVID-19 - participant should respond
considering whether the sign/symptom was recurrent or per-
sistent from the day of remission of the disease to the cur-
rent day (day of data collection).
Data were tabulated and statistically analyzed using SPSS
25.0. The inferential analysis was performed using the
Friedman test to compare the results obtained with the SSL
before, during, and after COVID-19. Multiple pairwise
comparisons with Bonferroni corrections were performed
for cases of significance. Multiple linear regression with the
selection of variables by the stepwise method was performed
to analyze the factors related to the maintenance of symp-
toms after COVID-19. For all inferential analyses, a signifi-
cance level of 5% was adopted.
RESULTS
Forty-five individuals participated in this study, with a
mean age of 44 years and 10 months, 24 females and 21
males. The descriptions of the other variables independent
of sociodemographic data, disease course, and vocal com-
plaints are shown in Tables 1 and 2.
TABLE 1.
Descriptive Analysis of Independent Quantitative Variables
Variable Mean SD Minimum Maximum 1Q Median 3Q
Age 44.89 13.15 19.00 78.00 35.50 45.00 55.50
Body mass index 29.76 5.26 20.28 42.27 25.90 30.61 33.53
Time since COVID-19 diagnosis (in days) 41.91 17.19 19.00 107.00 30.00 38.00 47.50
Days of hospitalization 1.29 2.77 0.00 13.00 0.00 0.00 0.50
Days of ICU stay 0.51 1.84 0.00 10.00 0.00 0.00 0.00
Descriptive analysis.
SD, standard deviation; 1Q, first quartile; 3Q, third quartile.
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2Journal of Voice, Vol. &&, No. &&, 2021

Table 3 shows descriptive analysis regarding the presence
or absence of the 14 vocal signs and symptoms investigated
in the SSL. The vocal signs and symptoms most commonly
reported before COVID-19 were phlegm (26.67%; n=12)
and dry throat (24.44%; n=11). During COVID-19, the
most frequent vocal signs and symptoms were tired or
changed voice after use for a short time (73.33%; n=33) and
dry throat (71.11%; n=32). After COVID-19, the most
reported vocal signs and symptoms were dry throat
(57.78%; n=26) and phlegm (53.33; n=24).
Table 4 indicates a significant difference in self-perception
of vocal signs and symptoms before, during, and after
COVID-19 (P<0.001). The self-perception of vocal signs
and symptoms before COVID-19 was lower than during (P
<0.001) and post-disease (P<0.001). Moreover, the self-
perception of vocal signs and symptoms after COVID-19
was lower than during the disease (P<0.001).
Regression to verify whether the variables (age, body
mass index, time since COVID diagnosis, days of hospitali-
zation, days of intensive care unit (ICU) stay, hospitaliza-
tion, noninvasive ventilation, oxygen therapy, smoking
history, vocal complaints before, during, and after COVID-
19), were related to self-perception of vocal signs and symp-
toms after COVID-19 resulted in a statistically significant
model (F(2,43) = 18.076; P<0.001; R2 = 0.422). Vocal
complaint after COVID-19 (b= 0.549; t = 4.508; P<0.001)
and oxygen therapy (b= 0.333; t = 2.737; P= 0.009) were
predictors of self-perception of vocal signs and symptoms
after having COVID-19 (Table 5).
DISCUSSION
Understanding the impact of COVID-19 on voice and com-
munication is extremely important for speech therapists
to develop appropriate and resolutive actions for the
population.
The types of signs and symptoms most reported during
and after COVID-19 are related to pulmonary and
TABLE 2.
Descriptive Analysis of Independent Binary Nominal
Binary Variables
Variable No Yes
n%n%
Hospitalization 31 68.89 14 31.11
Noninvasive ventilation 44 97.78 1 2.22
Oxygen therapy 36 80.00 9 20.00
Smoking history 35 77.78 10 22.22
Vocal complaints before
COVID-19
40 88.89 5 11.11
Vocal complaints during
COVID-19
21 46.67 24 53.33
Vocal complaints after
COVID-19
31 68.89 14 31.11
Descriptive analysis.
n, absolute frequency; %, relative frequency.
TABLE 3.
Descriptive Analysis of Binary Nominal Qualitative Vari-
ables Related to SSL, in the Pre, During, and After
COVID-19 Timepoints
Symptoms Before During After
n%n%n%
Hoarseness
No 39 86.67 23 51.11 33 73.33
Yes 6 13.33 22 48.89 12 26.67
Voice becoming
tired or change
after use for a
short time
No 43 95.56 12 26.67 30 66.67
Yes 2 4.44 33 73.33 15 33.33
Trouble singing
or speaking
low
No 44 97.78 34 75.56 38 84.44
Yes 1 2.22 11 24.44 7 15.56
Difficulty in pro-
jecting your
voice
No 42 93.33 25 55.56 36 80.00
Yes 3 6.67 20 44.44 9 20.00
Difficulty singing
high
No 45 100.00 34 75.56 39 86.67
Yes 0 0.00 11 24.44 6 13.33
Discomfort
when speaking
No 45 100.00 26 57.78 40 88.89
Yes 0 0.00 19 42.22 5 11.11
Monotone voice
No 43 95.56 31 68.89 41 91.11
Yes 2 4.44 14 31.11 4 8.89
Effort to speak
No 45 100.00 23 51.11 39 86.67
Yes 0 0.00 22 48.89 6 13.33
Dry throat
No 34 75.56 13 28.89 19 42.22
Yes 11 24.44 32 71.11 26 57.78
Sore throat
No 40 88.89 25 55.56 38 84.44
Yes 5 11.11 20 44.44 7 15.56
Phlegm
No 33 73.33 16 35.56 21 46.67
Yes 12 26.67 29 64.44 24 53.33
Acidic or bitter
taste in the
mouth
No 40 88.89 18 40.00 28 62.22
Yes 5 11.11 27 60.00 17 37.78
Difficulty
swallowing
No 44 97.78 35 77.78 43 95.56
Yes 1 2.22 10 22.22 2 4.44
(Continued)
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Ana Paula Dassie-Leite, et al Vocal Signs and Symptoms Related to COVID-19 and Risk Factors for their Persiste 3

laryngeal aspects. The most common symptom reported
during the pandemic was tired or changed voice after use
for a short time (73.33%; n=33). This symptom persisted in
33.3% of individuals after COVID-19, and only 4.4% of
patients reported it before COVID-19. This symptom is
directly associated with respiratory sequelae related to the
disease, and its persistence refers to the maintenance of
fatigue symptoms, pointed out in the literature as the most
frequent symptom type after COVID-19.
20
Pulmonary func-
tion is directly related to subglottic airflow, which is funda-
mental for phonation and pneumo-phono-articulatory
coordination.
21−25
The dry throat and phlegm symptoms are related to dehy-
dration and inflammatory processes in the upper airways
and vocal folds.
26,27
In general, symptoms related to vocal
tract sensations have been observed in other studies investi-
gating patients with COVID-19 at varying frequencies.
28−31
Otorhinolaryngological symptoms, in general, may be pres-
ent in almost 60% of patients during the disease.
30
Cough is
one of the most common symptoms of the disease and may
be present in approximately 76% of cases,
29
causing irrita-
tion, edema, and even phonotrauma in the vocal folds.
Regarding the period after COVID-19, there is a possibility
that 25% of individuals will continue experiencing laryngeal
sensitivity.
11
This study hypothesized that respiratory sequelae and
vocal tract symptoms related to COVID-19 might be risk
factors for the development of dysphonia. This study
indicates that hoarseness was present in 48.89% of the cases
during the disease, higher rates than those described in the
literature regarding dysphonia, which is 27%.
12
In this
study, 26.67% of patients presented with symptoms of
hoarseness after the disease. No specific studies on this
symptom were found, but the results are compatible with
those of a study that showed that approximately 25% of
patients reported persistent vocal changes after the
disease.
11
Some atypical cases of dysphonia during or after
COVID-19 have been reported, including vocal fold immo-
bility, paradoxical movement of vocal folds, and psycho-
genic dysphonia.
12,28,32
For this reason, in addition to the
possibility of vocal disorders due to respiratory sequelae or
vocal tract symptoms commonly related to the disease, each
case must be analyzed individually according to clinical his-
tory and vocal manifestations.
The highest frequency of vocal signs and symptoms was
observed during COVID-19, with differences compared to
those before and during the disease. The frequency of vocal
signs and symptoms after COVID-19, although lower than
during COVID-19, was higher than that before COVID-19.
Thus, it was confirmed that many signs and symptoms per-
sisted even after curing the disease. A median of one symp-
tom was noted before COVID-19, which is compatible with
TABLE 3. (Continued )
Symptoms Before During After
n % n%n%
Voice instability
or tremor
No 45 100.00 35 77.78 39 86.67
Yes 0 0.00 10 22.22 6 13.33
Descriptive analysis.
n, absolute frequency; %, relative frequency.
TABLE 4.
Comparison of Self-Perception of Vocal Signs and Symptoms Before, During and After Having COVID-19
Variables Mean SD Minimum Maximum 1Q Median 3Q X
2
P-value Pairwise
Vocal signs and symp-
toms
before COVID-19
1.09 1.39 0 6.00 0.00 1.00 1.00 66.53 <0.001 Before <During (P<
0.001)
= After (P<0.001);
After <During (P<
0.001)
Vocal signs and symp-
toms
during COVID-19
6.22 3.63 0 14.00 3.00 7.00 8.50
Vocal signs and symp-
toms
after a COVID-19
3.24 3.00 0 12.00 1.00 3.00 4.00
Friedman test; multiple comparations by pairwise with Bonferroni correction.
SD, standard deviation; 1Q, first quartile; 3Q, third quartile.
TABLE 5.
Multiple Linear Regression Model of Independent Varia-
bles as Predictors of Self-Perception of Vocal Signs and
Symptoms After Having COVID-19
Model B btP-value VIF
(Constant) 1.622 3.323 0.002
Vocal com-
plaints after
COVID-19
3.649 0.549 4.508 <0.001 1.001
Oxygen therapy 2.495 0.333 2.737 0.009 1.001
Multiple linear regression, stepwise method.
r
2
= 0.422.
VIF, Variance inflation factor.
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4Journal of Voice, Vol. &&, No. &&, 2021

that in the general population.
18
The median of seven vocal
signs and symptoms during COVID-19 was compatible
with the numbers presented for individuals with dysphonia
in general.
18
After COVID-19, the median of three symp-
toms, although lower than that commonly presented by
individuals with vocal disorders,
18
is similar to that pre-
sented by Brazilian teachers, a group whose profession his-
torically indicates the presence of great symptomatology
and vocal risk.
19
Individuals who used oxygen therapy had a higher fre-
quency of vocal signs and symptoms after COVID-19. The
prescription of oxygen therapy is widely described in the lit-
erature to treat respiratory failure as it improves O
2
supply
to cells by increasing the partial pressure of oxygen in the
arterial blood through a higher oxygen concentration in the
inspired air.
33−36
In cases of COVID-19, it is a frequently
used and important procedure for recovery.
37,38
One of the
side effects of this type of therapy is the dryness due to inad-
equate humidification.
39
Dryness of the mucous membranes
of the vocal tract can be hypothesized as a cause, and dehy-
dration may increase vocal symptomatology.
Individuals with vocal complaints after COVID-19 also
had a higher frequency of vocal signs and symptoms. This
result was expected, and there is already a consensus on this
aspect in the literature.
40−42
This study presented a risk of memory bias due to data
collection performed after COVID-19 from the moments
before and during the disease. For a better understanding of
the theme, studies with longitudinal follow-up of patients
after COVID-19 in monitoring vocal symptoms and clinical
data of auditory-perceptual, acoustic, aerodynamic, and lar-
yngological evaluations are suggested; analysis of vocal data
of COVID-19 patients submitted to invasive mechanical
ventilation; and investigation of the effects of speech ther-
apy and its association with respiratory physiotherapy on
patients’vocal rehabilitation after COVID-19.
CONCLUSION
Individuals affected by COVID-19 have a higher frequency
of signs and symptoms during the disease; however, they
still maintain a higher frequency than baseline after remis-
sion. The most reported vocal signs and symptoms during
and after COVID-19 indicate a relationship with pulmonary
sequelae and upper airway, and vocal symptoms commonly
present in the acute phase of the disease. The need for oxy-
gen therapy may indicate a risk for a higher occurrence of
after COVID-19 vocal signs and symptoms.
DECLARATION OF COMPETING INTEREST
There are no conflicts of interest to declare.
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