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RELATION BETWEEN OROTRACHEAL INTUBATION, INFLAMMATORY MARKERS, BREATHING AND VOICE IN POST-COVID-19

  • Thaís Dias Feltrin
    Correspondence
    Corresponding author: Thaís Dias Feltrin. Av. Roraima nº 1000, Building 26D, room 1441, Cidade Universitária, Bairro Camobi, Santa Maria - RS, CEP: 97105-900, University of Santa Maria/RS.
    Affiliations
    Master in Human Communication Disorders, Federal University of Santa Maria, Santa Maria, RS, Brazil
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  • Carla Aparecida Cielo
    Affiliations
    PhD in Linguistics and Letters, Professor at the Department of Speech Therapy and the Graduate Program in Human Communication Disorders - Federal University of Santa Maria, Santa Maria (RS), Brazil
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  • Adriane Schmidt Pasqualoto
    Affiliations
    PhD in Pulmonary Sciences, Professor at the Department of Physiotherapy and the Graduate Program in Human Communication Disorders, Federal University of Santa Maria, Santa Maria, RS, Brazil.
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Published:February 22, 2023DOI:https://doi.org/10.1016/j.jvoice.2023.02.015
RELATION BETWEEN OROTRACHEAL INTUBATION, INFLAMMATORY MARKERS, BREATHING AND VOICE IN POST-COVID-19
Previous ArticleComparative Results of Vocal Fold Injury According to the Fiber-Based Laser in a Rabbit Vocal Fold Model
Next ArticleVariability in Voice Characteristics of Female Speakers With Phonotraumatic Vocal Fold Lesions

      Abstract

      Introduction

      COVID-19, an infectious disease with a wide spectrum of clinical manifestations and intensities in the human body, it can cause respiratory and vocal disorders, with fatigue.

      Objective

      To verify the relation between biological Inflammatory markers D-dimers and C-Reactive Protein, Forced Vital Capacity, Maximum Phonation Time, vocal performance and fatigue, length of hospitalization period and gender of people affected by COVID-19 who were hospitalized, but did not use orotracheal intubation and compare with a group of post-COVID-19 patients with orotracheal intubation.

      Methods

      Data on D-dimers and C-Reactive Protein, spirometry, Maximum Phonation Time, performance and vocal fatigue were collected. The study included 42 adult people affected by COVID-19 who were hospitalized, 22 (52.4%) female and 20 (47.6%) male; 23 (54.8%) critical cases composing the group with orotracheal intubation (average age 48.9 years old) and 19 (45.24%) severe cases in the group without orotracheal intubation (average age 49.9 years old). Results: hospital length of stay was significantly longer for the group with orotracheal intubation; D-dimers were significantly altered in all groups; correlations between maximum phonation times were positive and significant; correlations between maximum phonation times, vocal performance and fatigue were both negative and significant.

      Conclusion

      Patients with orotracheal intubation had longer hospital internment and increased D-dimers and were amazed that, whenever maximum phonation times decreased performance and vocal fatigue increased.

      Keywords

      Introduction

      COVID-19 (coronavirus disease 2019) is an infectious disease caused by the new coronavirus (SARS-CoV-2), associated with its most serious complication, severe acute respiratory syndrome 2

      World Health Organization. WHO. Coronavirus disease (COVID-19) outbreak. Published 2020. (https://www.who.int).

      . It develops in the human body with repercussions on breathing and voice
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      . Once the inflammatory condition in the body is determined by COVID-19, the person may evolve well, may need non-invasive ventilatory support, or present worsening and necessity of orotracheal intubation (OTI).
      Aspects related to sex and COVID-19 vary according to the location in which the studies were carried out, but in general the disease affects more males
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      • Huang C
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      . In addition, older age, high number of comorbidities such as obesity, diabetes, heart failure, prominent laboratory abnormalities were associated with critically ill patients and longer hospitalization periods
      • Zhang JJ
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      • Caruso D
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      In some post-COVID-19 cases during follow-up, it appears that patients may have clinical complications related to the disease itself, the decompensation of the underlying disease and the instituted treatment
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      , such as lung damage that triggers respiratory failure and in an attempt to repair these damages, patients can evolve to pulmonary fibrosis
      • Wei J
      • Yang H
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      • Fan B
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      Analysis of thin-section CT in patients with coronavirus disease (COVID-19) after hospital discharge.
      Clinical Imaging. 2020; 28: 383-389https://doi.org/10.3233/XST-200685
      . The reflexes of these alterations can appear in the voice, more specifically in the maximum phonation times (MPT), which are influenced by the Forced vital capacity (FVC) or by the inadequate laryngeal valve effect
      • Lechien JR
      • Chiesa-Estomba CM
      • Place S
      • Van Laethem Y
      • et al.
      Features of Mild-to-Moderate COVID-19 Patients With Dysphonia.
      J Voice. 2022; 36: 249-255https://doi.org/10.1016/j.jvoice.2020.05.012
      ,
      • Wichmann D
      • Sperhake JP
      • Lütgehetmann M
      • Steurer S
      • et al.
      Autopsy Findings and Venous Thromboembolism in Patients With COVID-19: A Prospective Cohort Study.
      Ann Intern Med. 2020; 173: 268-277https://doi.org/10.7326/M20-2003
      , and in the increase of vocal fatigue.
      The change in glottic coaptation may be caused by the elevated expression of angiotensin-converting enzyme 2 (ACE-2) that has been found in the vocal fold epithelium in individuals with COVID-19 causing edema
      • Lechien JR
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      Features of Mild-to-Moderate COVID-19 Patients With Dysphonia.
      J Voice. 2022; 36: 249-255https://doi.org/10.1016/j.jvoice.2020.05.012
      . OTI can injure the vocal folds, impairing glottic closure. They can be detected in patients with intubation for periods longer than 24 hours. Lesions occur mainly due to the pressure exerted by tubes larger than 7mm and/or cuff on the laryngotracheal mucosa and/or with the tube angle in relation to the labial commissure different from 90°
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      .
      They are correlated with a greater occurrence of dysphagia and greater degrees of vocal alteration. Clinical signs after extubation are: dysphagia, odynophagia, dysphonia/hoarseness, presence of stridor, pain on palpation in the trachea region and presence of bleeding
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      Despite the use of vaccines and preventive measures, many people still end up being (re)infected and develop changes after COVID-19. Therefore, the importance of verifying the existence of a relation between post-COVID-19 inflammatory, respiratory and vocal variables to reduce the risk of other problems in the general health of the population.
      Knowing the relation of biological markers with VC, MPT and between performance and vocal fatigue, assists speech therapy care to be personalized and assertive, reducing hospitalization time, hospital costs, the risk of laryngeal injuries, with consequences on communication, which may interfere in the quality of life of patients and cause harm to society as a whole
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      .
      Thus, the working hypothesis of this research was that the people in the sample would have a predominance of OTI, male gender, older age and higher values ​​in the biological markers of inflammation CRP as well as DD and would tend to have a lower VC, since the lung is one of the organs more affected, with lower MPT, higher performance scores and vocal fatigue, along with longer hospitalization.
      Based on the above, the objective of this study was to verify the relation between the biological markers of inflammation DD and CRP, VC, MPT, vocal performance and fatigue, furthermore gender of people affected by COVID-19 who were hospitalized, but did not use the OTI to compare with a group of post-COVID-19 patients with OTI.

      Materials and Methods

      This is a cross-sectional, observational, field research, prospective, comparative and quantitative study, approved by the Human Research Ethics Committee of the institution of origin (n 4.527.287). The data were collected at the post-COVID-19 Rehabilitation Outpatient Clinic of the University Hospital of Santa Maria/RS, from August 2021 to May 2022.

      Sampling Process

      At the time of hospital discharge, patients returned for reassessment with the Pulmonologist. When the patient attended this return visit, he was referred to the Post-COVID-19 Rehabilitation Outpatient Clinic. If the doctor from another specialty had performed the discharge and had not scheduled a reassessment at the hospital, a nurse carried out an active search in the digital medical records of these patients and, after being contacted, they were invited to participate in this research. At that moment of invitation, all ethical aspects were clarified and, if they were interested in participating, they should sign the informed consent form and go through the processes described below.
      It is also important to add that the time for each assessment varied between 15 and 45 minutes, since most of them depended on the understanding and collaboration of the patient. To complete all assessments, the patient attended the medical clinic on two or three occasions.
      The inclusion criteria adopted for patient selection were: male or female genders; ages between 20 and 65 years to exclude vocal changes and presbyphonia
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      ; having been admitted to the UHSM with a medical diagnosis of COVID-19 with or without OTI. As exclusion criteria were adopted: report or diagnosis of neurological, endocrinological, psychiatric, gastric or laryngeal or vocal changes prior to COVID-19; not passing the audiological screening; declaring oneself to be a smoker or alcoholic and not having complete data in the medical records. For the application of the inclusion and exclusion criteria, the procedures described below were performed with the patients.

      Anamnesis

      Patients underwent anamnesis to report items such as: sex; age; pre-existing diseases (systemic or neurological); the hospital length of stay; respiratory, auditory and vocal symptoms, as well as smoking and alcoholism. The data were collected at the post-COVID-19 Rehabilitation Outpatient Clinic of the University Hospital of Santa Maria/RS.

      Audiological Screening

      The patients were submitted to audiological screening, without meatoscopy, performed by airborne pure tone scanning making use of earphones at frequencies of 1000, 2000 and 4000 Hz at 25 dB, with a calibrated audiometer (Interacoustics, AD629) and in an acoustic booth
      American Speech-Language-Hearing Association
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      , not having DD

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      , not having CV

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      , having discomfort during voice collection

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      , failure in the hearing screening
      • Baj J
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      • Buszewicz G
      • et al.
      COVID-19: Specific and Non-Specific Clinical Manifestations and Symptoms: The Current State of Knowledge.
      J Clin Med. 2020; 9: 1753https://doi.org/10.3390/jcm9061753
      , did not answer the questionnaires
      • Lechien JR
      • Chiesa-Estomba CM
      • Place S
      • Van Laethem Y
      • et al.
      Features of Mild-to-Moderate COVID-19 Patients With Dysphonia.
      J Voice. 2022; 36: 249-255https://doi.org/10.1016/j.jvoice.2020.05.012
      . Eighteen female subjects were excluded for: not having the PCR

      World Health Organization. WHO. Coronavirus disease (COVID-19) outbreak. Published 2020. (https://www.who.int).

      , not having the DD
      • Wichmann D
      • Sperhake JP
      • Lütgehetmann M
      • Steurer S
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      Autopsy Findings and Venous Thromboembolism in Patients With COVID-19: A Prospective Cohort Study.
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      , not having the PCR or the DD
      • Lechien JR
      • Chiesa-Estomba CM
      • Place S
      • Van Laethem Y
      • et al.
      Features of Mild-to-Moderate COVID-19 Patients With Dysphonia.
      J Voice. 2022; 36: 249-255https://doi.org/10.1016/j.jvoice.2020.05.012
      , not having the VC
      • Gardenghi G.
      Pathophysiology of worsening lung function in COVID-19.
      Rev Bras de Fisiologia do Exercício. 2020; 19 (Supl. COVID-19)https://doi.org/10.33233/rbfe.v19i2.4058
      , having discomfort during vocal collection
      • Lechien JR
      • Chiesa-Estomba CM
      • Place S
      • Van Laethem Y
      • et al.
      Features of Mild-to-Moderate COVID-19 Patients With Dysphonia.
      J Voice. 2022; 36: 249-255https://doi.org/10.1016/j.jvoice.2020.05.012
      , failed hearing screening
      • Lechien JR
      • Chiesa-Estomba CM
      • Place S
      • Van Laethem Y
      • et al.
      Features of Mild-to-Moderate COVID-19 Patients With Dysphonia.
      J Voice. 2022; 36: 249-255https://doi.org/10.1016/j.jvoice.2020.05.012
      or did not answer the questionnaires
      • Gardenghi G.
      Pathophysiology of worsening lung function in COVID-19.
      Rev Bras de Fisiologia do Exercício. 2020; 19 (Supl. COVID-19)https://doi.org/10.33233/rbfe.v19i2.4058
      .
      Subjects who passed the inclusion and exclusion criteria made up the study sample and were divided into CG (critical group, subjects who required OTI) and SG (severe group, subjects who did not require OTI). So far, the study sample consisted of 42 cases, 22 (52.38%) females and 20 (47.62%) males, and 23 (54.76%) CG (mean age 48.86 years) and 19 (45.24%) SG (mean age 49.89 years). At the time of data collection for our study, no patient had a tracheostomy.
      The Sample Power method of Minitab v21.2 software was applied to determine the power of this sample of all 42 cases. For this, we considered the prevalence of OTI in the sample, which was 54.8% (23 cases with OTI). The sample power of this study was 0.7405 (74.05%), a value slightly below the ideal value, which is 0.80 (80%).
      After the contraction process, the following procedures were performed with the patients:

      Data Collection

      For data collection, measurements of the MPT/a/, /s/ and /z/ were performed and the Vocal Performance Questionnaire (VPQ) and Vocal Fatigue Index (VFI) protocols were applied. Data were collected by different evaluators, in a standardized manner, following the protocol of the clinic.
      The results of the CRP, DD and spirometry measurements, as well as information on the hospital length of stay (LoS) and use of OTI were consulted in the medical records of each post-COVID-19 patient, as they are part of the Rehabilitation Clinic post-COVID-19 routine of UHSM. Following the recommendations of the competent bodies

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      ,

      Empresa Brasileira de Serviços Hospitalares. EBSERH. Protocolo de higienização das mãos. Brasília. p. 1-29, 2020. (http://www2.ebserh.gov.br/documents/16496/4822709/PRT+Higiene+de+m%C3%A3os+2020.pdf/d2e4ff27-32e7-4b91-ae28-2736597cfd97).

      ,

      Centers for disease control and prevention. CDC. Infection Control: Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) | CDC, fev. 2021. (https://www.cdc.gov/coronavirus/2019-ncov/hcp/infection-control-recommendations.html?CDC_AA_refVal=https/3A/2F/2Fwww.cdc.gov/2Fcoronavirus/2F2019-ncov/2Finfection-contro/2Fcontrol-recommendations.html#take_precautions).

      , safety measures were adopted during data collection for this research, especially to keep patient safety
      • Sanitária Agência Nacional de Vigilância
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      ANVISA, Brasília2009
      http://bvsms.saude.gov.br/bvs/publicacoes/seguranca_paciente_servicos_saude_higienizacao_maos.pdf
      .

      Maximum phonation times

      All MPT emissions were collected twice in a place with ambient noise lower than 48 dBC, measured by a digital sound pressure level meter (Icel®, DL 4200)
      • Patel RR
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      • Švec JG
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      . The subjects were instructed to sustainably emit the phonemes /a/, /s/ and /z/ in usual pitch and loudness, in the orthostatic position after deep inspiration, until the end of expiration. The MPT were performed in the audiology sector, as it is an acoustically treated environment at the UHSM.
      For further analysis, the highest timed value of each phoneme in seconds (s) was used
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      . MPT/a/ values ​​between 14.04 and 26.96 s were considered reference values ​​for adult females and between 16.06 and 26.27 s for adult males
      • Beber BC
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      . Reference values ​​for both sexes of MPT/s/ and /z/ range from 15 to 25 s
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      . Lower values ​​were suggestive of air escape during phonation (lack of glottic coaptation and/or respiratory flow or control) and higher values ​​were suggestive of glottic hyperfunction
      • Beber BC
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      • Behlau M
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      Revinter, Rio de Janeiro2013: 85-245
      .

      Vocal self-assessment protocols

      The vocal self-assessment questionnaires were read by the patients and the answers marked by the individuals themselves, leaving the researchers available to clarify possible filling doubts
      • Zambon F
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      • Cielo CA
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      . The data were collected at the post-COVID-19 Rehabilitation Outpatient Clinic of the University Hospital of Santa Maria/RS (UHSM).
      The VPQ protocol is derived from clinical practice
      • Carding PN
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      J Laryngol Otol. 2009; 123: 823-829https://doi.org/10.1017/S0022215109005398
      , translated and validated into Brazilian Portuguese
      • Paulinelli BR
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      • Behlau M.
      Validação do Questionário de Performance Vocal no Brasil.
      Rev Soc Bras Fonoaudiol [online]. 2012; 17: 85-91https://doi.org/10.1590/S1516-80342012000100016
      , and includes several aspects of vocal performance, with 12 questions. The patient chose the best option among the five alternatives, with the letter “a” corresponding to one point up to a maximum of five points in the letter “e”. The maximum sum of points is 60 and the minimum score considered normal is less than 12, any value above 12 indicates a decrease in vocal performance. It is a short, convenient questionnaire and has high internal consistency to measure the degree of vocal deviation
      • Carding PN
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      J Voice. 1999; 13: 72-104https://doi.org/10.1016/s0892-1997(99)80063-0
      .
      The VFI consists of 17 questions, divided into four vocal factors
      • Zambon F
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      • Nanjundeswaran C
      • et al.
      Vocal fatigue index: Validation and cut-off values off the Brazilian version.
      J. Voice. 2022; 36: 434.E17-434.E24https://doi.org/10.1016/j.voice.2020.06.018
      . Factor 1 has seven items (items 2, 3, 4, 5, 9, 10 and 11) related to “Tiredness and voice impairment”; factor 2 has three items (items 1, 6 and 7) related to "Avoidance of voice use"; factor 3 has four items (items 13, 14, 15 and 16) related to "Physical discomfort"; and factor 4 has three items (items 17, 18 and 19) related to "Improvement of voice symptoms with rest". The protocol was answered by the patient himself, according to the frequency with which he experiences the symptoms: 0 = never, 1 = almost never, 2 = sometimes, 3 = almost always and 4 = always. The threshold values ​​for each factor were: 4.5 for tiredness and voice impairment; 3.5 for avoidance of voice usage; 1.5 for physical discomfort and 8.5 for improvement of vocal symptoms with rest. The threshold value for the total score was 11.5. The score is obtained by the simple sum of the questions. Therefore, the higher the score, the greater the fatigue in the first three factors. Unlike the other domains, the higher the score for the fourth factor, the greater the improvement in symptoms (
      • Zambon F
      • Moreti F
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      • Nanjundeswaran C
      • et al.
      Vocal fatigue index: Validation and cut-off values off the Brazilian version.
      J. Voice. 2022; 36: 434.E17-434.E24https://doi.org/10.1016/j.voice.2020.06.018
      ,
      • Abou-Rafée M
      • Zambon F
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      • Behlau M.
      Fadiga vocal em professores disfônicos que procuram atendimento fonoaudiológico.
      CoDAS [online]. 2019; 31e20180120https://doi.org/10.1590/2317-1782/20182018120
      ,
      • Depolli GT
      • Fernandes DNS
      • Costa MRB
      • Coelho SC
      • et al.
      Fadiga e Sintomas Vocais em Professores Universitários.
      Distúrbios Comum. 2019; 31: 225-233https://doi.org/10.23925/2176-2724.2019v31i2p225-233
      ,
      • Hunter EJ
      • Banks RE.
      Gender Differences in the Reporting of Vocal Fatigue in Teachers as Quantified by the Vocal Fatigue Index.
      Ann Otol Rhinol Laryngol. 2017; 126: 813-818https://doi.org/10.1177/0003489417738788
      ,
      • Hunter EJ
      • Maxfield L
      • Graetzer S.
      The Effect of Pulmonary Function on the Incidence of Vocal Fatigue Among Teachers.
      J Voice. 2020; 34: 539-546https://doi.org/10.1016/j.jvoice.2018.12.011
      ,
      • Nanjundeswaran C
      • Jacobson BH
      • Gartner-Schmidt J
      • Verdolini Abbott K
      Vocal Fatigue Index (VFI): Development and Validation.
      J Voice. 2015; 29: 433-440https://doi.org/10.1016/j.jvoice.2014.09.012
      ,
      • Vitor JS
      • Antonetti AES
      • Moreira PAM
      • Ribeiro VV
      • et al.
      Fadiga vocal e qualidade de vida em voz na disfonia comportamental.
      Anais. Bauru: Faculdade de Odontologia de Bauru. 2018. 2018
      https://repositorio.usp.br/item/002931073
      ,
      • Zambon F
      • Moreti F
      • Nanjundeswaran C
      • Behlau M
      Equivalência cultural da versão brasileira do Vocal Fatigue Index – VFI.
      CoDAS [online]. 2017; 29e20150261https://doi.org/10.1590/2317-1782/20172015261
      ).

      Spirometry

      Spirometry is a physiological test that measures the maximum volume of air that an individual can inhale and exhale with maximum effort. The primary signal measured in spirometry is volume or flow as a function of time
      • Graham BL
      • Steenbruggen I
      • Miller MR
      • Barjaktarevic IZ
      • et al.
      Standardization of Spirometry 2019 Update. An Official American Thoracic Society and European Respiratory Society Technical Statement.
      Am J Respir Crit Care Med. 2019; 200: e70-e88https://doi.org/10.1164/rccm.201908-1590ST
      . The most relevant measure discussed in this document is the FVC, which is the volume released during an expiration performed as vigorously and completely as possible starting from the complete inspiration
      • Graham BL
      • Steenbruggen I
      • Miller MR
      • Barjaktarevic IZ
      • et al.
      Standardization of Spirometry 2019 Update. An Official American Thoracic Society and European Respiratory Society Technical Statement.
      Am J Respir Crit Care Med. 2019; 200: e70-e88https://doi.org/10.1164/rccm.201908-1590ST
      ,
      • Pereira CA
      Espirometria. In: Sociedade Brasileira de Pneumologia e Tisiologia. Diretrizes para Testes de Função Pulmonar.
      J Pneumol. 2002; 28: S1-S82
      https://cdn.publisher.gn1.link/jornaldepneumologia.com.br/pdf/Suple_139_45_11%20Espirometria.pdf
      . A digital spirometer was used (MS-IOS, Jaeger).
      The subject was seated using a clip for nasal occlusion and the lips should completely occlude the disposable mouthpiece inserted in the turbine. After being well positioned, the subject was instructed to perform both maximum inspiration and expiration maneuvers, according to the recommendations of the Brazilian Society of Pulmonology and Phthisiology
      • Pereira CA
      Espirometria. In: Sociedade Brasileira de Pneumologia e Tisiologia. Diretrizes para Testes de Função Pulmonar.
      J Pneumol. 2002; 28: S1-S82
      https://cdn.publisher.gn1.link/jornaldepneumologia.com.br/pdf/Suple_139_45_11%20Espirometria.pdf
      until three reproducible maneuvers were recorded
      • Awan SN
      • Novaleski CK
      • Yingling JR.
      Test-retest reliability for aerodynamic measures of voice.
      J Voice. 2013; 27: 674-684https://doi.org/10.1016/j.jvoice.2013.07.002
      . The VC spirometric data were interpreted making use of the Pereira
      • Pereira CA
      Espirometria. In: Sociedade Brasileira de Pneumologia e Tisiologia. Diretrizes para Testes de Função Pulmonar.
      J Pneumol. 2002; 28: S1-S82
      https://cdn.publisher.gn1.link/jornaldepneumologia.com.br/pdf/Suple_139_45_11%20Espirometria.pdf
      normative values ​​for the Brazilian Society of Pulmonology and Phthisiology, the Forced vital capacity (FVC) is normally equal to the slow vital capacity (SVC)
      • Menna Barreto SS
      Volumes Pulmonares.In: Sociedade Brasileira de Pneumologia e Tisiologia. Diretrizes para Testes de Função Pulmonar.
      J Pneumol. 2002; 28: S83-S94
      https://cdn.publisher.gn1.link/jornaldepneumologia.com.br/pdf/Suple_135_45_22%20volumes%20pulmonares.pdf
      ,
      • Pereira CAC
      • Moreira MA.
      Pletismografia – resistência das vias aéreas. . In: Sociedade Brasileira de Pneumologia e Tisiologia. Diretrizes para Testes de Função Pulmonar.
      J Pneumol. 2002; 28: S39-S54
      https://cdn.publisher.gn1.link/jornaldepneumologia.com.br/pdf/Suple_142_45_66%20Pletismografia.pdf
      ,
      • Pereira CAC
      • Duarte AAO
      • Gimenez A
      • Soares MR.
      Comparison between reference values for FVC, FEV|1, and FEV|1/FVC ratio in White adults in Brazil and those suggested by the Global Lung Function Initiative 2012.
      J Bras Pneumol. 2014; 40: 397-402https://doi.org/10.1590/S1806-37132014000400007
      ,
      • Pereira CAC.
      Difference between slow vital capacity and forced vital capacity in the diagnosis of airflow limitation.
      J Bras Pneumol. 2020; 46: 1-3
      http://www.jornaldepneumologia.com.br/details/3340/pt-BR/diferenca-entre-capacidade-vital-lenta-e-capacidade-vital-forcada-no-diagnostico-de-limitacao-ao-fluxo-aereo
      ,
      • Prata TA
      • Mancuzo E
      • Pereira CAC
      • Miranda SS
      • et al.
      Spirometry reference values for black adults in Brazil.
      J Bras Pneumol. 2018; 44: 449-455
      https://www.jornaldepneumologia.com.br/how-to-cite/2895/pt-BR/
      . In individuals without airflow obstruction, FVC and SVC should differ by less than 0.2 l. FVC greater than SVC means, in general, lack of collaboration in the slow maneuver. FVC may be less than SVC in individuals with an obstructive disorder (significant difference above 0.2 l).
      Spirometry was performed in the UHSM pneumology sector, but the spirometry results were consulted in the medical records of each post-COVID-19 patient, as they are part of the routine of the post-COVID-19 Rehabilitation Clinic of UHSM.

      Biological markers of inflammation

      Measurements of CRP and DD were consulted in the medical records of each post-COVID-19 patient, as they are part of the routine during hospitalization in the COVID-19 ward of the UHSM. In this study, for the analysis of the results, we considered that approximately 99% of the healthy population have CRP values ​​below 0.1 mg/dl and, in most cases, the levels do not reach 0.2 mg/dl
      • Ablij H
      • Meinders A.
      C-reactive protein: history and revival.
      Eur J Intern Med. 2002; 13: 412-422https://doi.org/10.1016/s0953-6205(02)00132-2
      . In general, mild inflammation and viral infections lead to elevations in the range of 0.1-0.4 mg/dl, while more severe inflammation and bacterial infections show serum concentrations between 0.40-20 mg/dl
      • Aguiar FJB
      • Ferreira-Júnior M
      • Sales MM
      • et al.
      Proteína C reativa: aplicações clínicas e propostas para utilização racional.
      Rev Assoc Med Bras. 2013; 59: 85-92
      https://www.scielo.br/pdf/ramb/v59n1/v59n1a16.pdf
      ,
      • Clyne B
      • Olsaker JS.
      The C-reactive protein.
      J Emerg Med. 1999; 17: 1019-1025https://doi.org/10.1016/S0736-4679(99)00135-3
      . The material used is the serum, the method is immunoturbidimetry with reference values ​​between 0.2 to 0.9 mg/dl.
      The reference value of DD in blood is up to 0.5 mcg/ml. In COVID-19, values ​​above 1 mcg/ml are associated with mortality and hypercoagulability
      • Bruno LC
      • Soares JAH
      • Lelis ESDS
      • Martins RM
      • et al.
      Dímero-D como importante marcador para estratificar a gravidade da infecção pelo novo coronavírus: revisão sistemática da literatura.
      Hematol Transfus Cell Ther. 2020; 42: 530-531https://doi.org/10.1016/j.htct.2020.10.895
      ,
      • Hayiroglu Mİ
      • Cinar T
      • Tekkeşin Aİ.
      Fibrinogen and D-dimer variances and anticoagulation recommendations in COVID-19: current literature review.
      Rev Assoc Med Bras. 2020; 66: 842-848https://doi.org/10.1590/1806-9282.66.6.842
      , which can be predictive of the severity of cases and longer hospitalization periods. The material used is plasma in citrate and the method is immunoturbidimetric with reference values ​​lower than 0.5 mcg/ml.

      Statistical methods

      The collected data were tabulated and statistically analyzed using the software: SPSS V20, Minitab 16 and Excel Office 2010. The significance level was 0.05 (5%). The Mann-Whitney U test was used to compare the CG across all the sample, segmented by gender. Comparison of the CG for the distribution of relative frequencies of qualitative factors was performed using Fisher's exact test. To analyze the relations between FVC, MPT, VFI and VPQ values, Spearman rank correlation was used. A significance level of p <0.05 was utilized.

      Results

      Comparisons between the variables age, hospital LoS and time until collection in the SG and CG, and in the entirety sample (All), according to gender are shown in Table 1. The hospital LoS was significantly longer for the CG (Female, Male and All).
      TABLE 1- Comparisons between the groups with and without orotracheal intubation for the variables age, length of hospitalization and time until the collect
      MeanMedianStandard Deviationp-value
      AgeFemaleCG47.44812.50.552
      SG51508.8
      MaleCG50.55180.941
      SG48.74913.8
      AllCG48.95110.50.781
      SG49.94911.2
      Hospital LoS (days)FemaleCG22.41812.5<0.001*
      SG9.2103.3
      MaleCG29.52315.90.002
      statistically significant p values; p<0.05
      SG12.3115.2
      AllCG25.82314.3<0.001
      statistically significant p values; p<0.05
      SG10.7104.5
      Time until collection (days)FemaleCG115.96695.20.974
      SG85.775.557.4
      MaleCG172.61241520.732
      SG16918297.8
      AllCG143981260.980
      SG125.28787.9
      Note: CG (critical group); SG (severe group); LoS, hospital length of stay.
      Mann-Whitney U test.
      low asterisk statistically significant p values; p<0.05
      Table 2 shows the comparisons between the CG and SG in the D-dimer and CRP variables according to gender and reference values. There was a statistically significant difference between the CG and SG in the distribution of DD in the totality of the sample.
      TABLE 2- Comparison between the groups with and without orotracheal intubation for the variables D-dimers and C-reactive protein, according to gender and reference values
      CGSGTotalp-value
      n%n%n%
      DD (mcg/ml)FemaleDeviant1191.76601777.30.096
      Normal18.3440522.7
      MaleDeviant11100888.919950.450
      Normal00111.115
      AllDeviant2295.71473.73685.70.043
      statistically significant p values; p<0.05
      Normal14.3526.3614.3
      PCR (mg/dl)FemaleDeviant1191.77701881.80.197
      Normal18.3330418.2
      MaleDeviant1090.9910019950.550
      Normal19.10015
      AllDeviant2191.31684.23788.10.480
      Normal28.7315.8511.9
      Note: CG (critical group); SG (severe group); DD, D-dimer; PCR, C-reactive protein.
      Exact Test of Fisher.
      low asterisk statistically significant p values; p<0.05
      Table 3 shows the comparisons between the CG and SG in the variables VC and MPT/a/, MPT/s/ and MPT/z/, according to gender and reference values.
      TABLE 3- Comparison between the groups with and without orotracheal intubation for the variables forced vital capacity and maximum phonation times of /a/, /s/ and /z/, according to gender and reference values
      CGSGTotalp-value
      n%n%n%
      FVCFemaleDeviant216.7330522.70.301
      Normal1083.37701777.3
      MaleDeviant327.3222.25250.383
      Normal872.7777.81575
      AllDeviant521.7526.31023.80.729
      Normal1878.31473.73276.2
      MPT/a/FemaleReduced1191.78801986.40.351
      Normal18.3220313.6
      MaleReduced872.7666.714700.684
      Normal218.2111.1315
      Increased19.1222.2315
      AllReduced1982.61473.73378.60.699
      Normal313315.8614.3
      Increased14.3210.537.1
      MPT/s/FemaleReduced1191.77701881.80.357
      Normal18.3220313.6
      Increased0011014.5
      MaleReduced872.7777.815750.390
      Normal327.3111.1420
      Increased00111.115
      AllReduced1982.61473.73378.60.280
      Normal417.4315.8716.7
      Increased00210.524.8
      MPT/z/FemaleReduced121009902195.50.455
      Normal0011014.5
      MaleReduced763.6666.713650.156
      Normal436.4111.1525
      Increased00222.2210
      AllReduced1982.61578.934810.249
      Normal417.4210.5614.3
      Increased00210.524.8
      Note: CG (critical group); SG (severe group); FCV, Forced Vital Capacity; MPT, maximum phonation time of /a/, /s/ and /z/.
      Exact Test of Fisher.
      * statistically significant p values; p<0.05
      Table 4 shows the comparisons between the CG and SG in the VFI factors and VPQ according to gender and reference values.
      TABLE 4- Comparison between the groups with and without orotracheal intubation for the factors of the Vocal Fatigue Index and Vocal Performance Questionnaire, according to gender and reference values
      CGSGTotalp-value
      n%n%n%
      Factor 1 - Tiredness and voice impairmentFemaleDeviant758.35501254.50.309
      Normal541.75501045.5
      MaleDeviant218.2444.46300.179
      Normal981.8555.61470
      AllDeviant939.1947.41842.90.591
      Normal1460.91052.62457.1
      Factor 2 − Avoidance of voice useFemaleDeviant541.7440940.90.334
      Normal758.36601359.1
      MaleDeviant327.3333.36300.358
      Normal872.7666.71470
      AllDeviant834.8736.81535.70.890
      Normal1565.21263.22764.3
      Factor 3 − Physical discomfortFemaleDeviant6504401045.50.300
      Normal6506601254.5
      MaleDeviant327.3333.36300.358
      Normal872.7666.71470
      AllDeviant939.1736.81638.10.879
      Normal1460.91263.22661.9
      Factor 4 − Improvement of voice symptoms with restFemaleDeviant866.78801672.70.299
      Normal433.3220627.3
      MaleDeviant981.8777.816800.409
      Normal218.2222.2420
      AllDeviant1773.91578.93276.20.703
      Normal626.1421.11023.8
      VFI TotalFemaleDeviant758.344011500.236
      Normal541.76601150
      MaleDeviant545.5333.38400.308
      Normal654.5666.71260
      AllDeviant1252.2736.81945.20.320
      Normal1147.81263.22354.8
      VPQFemaleDeviant1210010100221001.000
      Normal000000
      MaleDeviant11100888.919950.450
      Normal00111.115
      AllDeviant231001894.74197.60.265
      Normal0015.312.4
      Note: CG (critical group); SG (severe group); VFI, vocal fatigue index; VPQ, vocal performance questionnaire.
      Exact Test of Fisher.
      * statistically significant p values; p<0.05
      Table 5 shows the correlations between VC, MPT, VFI and VPQ. The correlations between MPT, VFI and VPQ were statistically significant. The highest correlation occurred between VPQ and VFI, being positive and strong.
      TABLE 5- Correlations between Forced Vital Capacity, Maximum Phonation Times, Vocal Fatigue Index and the Vocal Performance Questionnaire
      VCMPT/a/MPT/s/MPT/z/VFI
      MPT/a/Corr (r)0.018
      p-valor0.909
      MPT/s/Corr (r)0.0470.556
      p-valor0.768<0.001*
      MPT/z/Corr (r)-0.0520.6990.711
      p-valor0.746<0.001
      statistically significant p values; p<0.05
      		<0.001*
      VFICorr (r)0.021-0.520-0.337-0.491
      p-valor0.895<0.001
      statistically significant p values; p<0.05
      		0.029*0.001*
      VPQCorr (r)0.019-0.486-0.277-0.4230.795
      p-valor0.9070.001*0.0760.005*<0.001*
      Note: FVC, Forced Vital Capacity; MPT, Maximum Phonation Time of /a/, /s/ and /z/; VFI, Vocal Fatigue Index; VPQ, Vocal Performance Questionnaire; Corr(r) - correlation.
      Spearman Correlation Test
      low asterisk statistically significant p values; p<0.05

      Discussion

      In our study, length of stay was significantly longer for the CG (Table 1), which is in line with the literature. Critical illness with the usage of mechanical ventilation can result in the weakness of acquisition and functional changes, increasing the length of hospitalization
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      . The MPT was significantly lower among survivors than among controls with average time of 15.97 s in the control group, 10.72 s in the pneumonia group and 8.88 s in the severe pneumonia group
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      . There was a higher frequency of persistent dysphonia in patients admitted to the ICU (71.4%) compared to patients in the wards (28.6%), but no statistically significant association was found between admission to the ICU and persistent dysphonia
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      As for OTI among hospitalized adults with COVID-19, there were high rates of dysphonia (42%) and dysarthria (23%) and the history of OTI was predictive of voice quality
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      . Voice-related complaints are the most common symptom, followed by those related to swallowing and breathing, and many were suggestive of OTI-related injury
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      . Other studies report that 53.7% of the analyzed patients had abnormal GRBAS scores and positive endoscopic findings correlated with self-reported VHI-10 scores
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      Prolonged OTI and tracheostomy during treatment of severe COVID-19 are major contributors to voice, airway, and swallowing dysfunction, laryngeal problems have also been identified in mild illness
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      . These complications are not limited to patients who needed OTI or tracheostomy, findings similar to ours, in which most patients had vocal disorders that were not restricted to OTI (Table 4). In our study, all CG subjects underwent OIT and, of these, four (17.39%) underwent tracheostomy. At the time of data collection for our study, no patient had a tracheostomy.
      When we observed the correlations between MPT, VFI and VPQ, the MPT showed a significant negative correlation with the VFI and VPQ, and VC did not significantly correlate with the other variables (Table 5). No other studies were found that correlated these variables in COVID-19. Despite that, similar studies reported that patients with a previous history of COVID-19 had significantly lower MPT, increased scores in questionnaires of self-reported voice complaints that revealed close correlations with the COVID-19 disease symptom scores, and the overall dysphonia severity score was higher in the study group than in the control group
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      .
      In disagreement with our data, previous studies concluded that as the MPT increases, the vital capacity also increases, evidencing the interrelation between these variables
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      . Likewise, it was observed that the greater the patient's VC is, the greater his MPT will be
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      .
      The innovative nature of relating OTI with inflammatory markers and vocal aspects, contribute to scientific evidence in the area and to society. As limitations, we highlight the small number of patients that did not allow stratification by age group, a long time after hospital discharge until the patient's evaluation, not being a multicenter study and, finally, the lack of comparison with a control group. Therefore, multicenter studies are suggested, with a control group, stratified by age correlating these variables plus other pulmonary, vocal and anthropometric measures, such as the body mass index.

      Conclusion

      Patients with OTI had a longer hospital stay and increased D-dimers and displayed that, whenever MPT decreased, vocal performance and fatigue increased.

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      Article info

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      Accepted: February 13, 2023

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      In Press Accepted Manuscript

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      DOI: https://doi.org/10.1016/j.jvoice.2023.02.015

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      © 2023 The Voice Foundation. Published by Elsevier Inc. All rights reserved.

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