key: cord-0731645-sj64zvf8
authors: Vance, Dylan; Shah, Priyanka; Sataloff, Robert T.
title: COVID-19: Impact on the Musician and Returning to Singing; A Literature Review
date: 2021-01-14
journal: J Voice
DOI: 10.1016/j.jvoice.2020.12.042
sha: 2e6b487731b0bc0d7f42ec30f469d4948f1a084d
doc_id: 731645
cord_uid: sj64zvf8

OBJECTIVE: The purpose of this study was to review current literature of the impact of COVID-19 on musicians and returning to singing. METHODS: A comprehensive search of peer-review articles was completed using PubMed, GoogleScholar, Scopus, and Web of Science. The search was completed using many key terms including voice, hoarseness, dysphonia, aphonia, cough, singers, and public speakers. The bibliography from each article found was searched to find additional articles. The search process revealed 56 peer-reviewed articles, 18 primary articles, ranging from the years 2019-2020. CONCLUSION: COVID-19 has had a major impact on singers and other musicians worldwide. It can of affect the voice and can lead to paresis/paralysis of laryngeal nerves to long-term changes in respiratory function. There is a risk from aerosolization/droplet formation transmission with singing, and with playing wind and brass instruments, that can be mitigated by following COVID-19 guidelines. Ways to reduce possible transmission during singing and instrument play include virtual rehearsals or performances, mask-wearing, instrument covers, smaller choirs, performing outside, excellent ventilation being socially-distanced, shorter rehearsals, regularly cleaning commonly-touched surfaces and washing hands, avoiding contact with others, and temperature screening.

Introduction COVID-19 symptoms include cough, dyspnea, fever, taste and smell dysfunction. Its effects on the voice and its impact on musicians and other professional voice user can be profound. This review examines existing knowledge on COVID-19's impact on the instrumentalist and singer to help guide future priorities for research, therapies, and criteria for returning to professional voice use.

A comprehensive search of peer-review articles was completed using PubMed, GoogleScholar, Scopus, and from Web of Science from the years 2019-2020. The search was completed using a many key terms including voice, hoarseness, dysphonia, aphonia, cough, singers, and public speakers. The bibliography from each article found was searched to find additional articles. The search process revealed 56 peer-reviewed articles, 18 primary articles, ranging from the years 2019-2020.

Impact on the Voice Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), which causes the disease COVID-19, can affect the voice. In a cohort of 702 American patients with mild-to-moderate symptoms from COVID-19, 26.8% experienced dysphonia 1 . This percentage is consistent with the 28.4% of patients with dysphonia in a cohort of 1420 European patients with mild-tomoderate symptoms 2 . The quality of the dysphonia varied. In a case series of 86 COVID-19 patients, 17 .1% had very mild dysphonia, 2.9% had mild or slight dysphonia, 2.9% had moderate dysphonia, and 1.4% had severe dysphonia. The remaining patients did not report dysphonia 3 . Dysphonia can result for several reasons. It is a relatively common symptom of viral infections of the upper respiratory tract and can be the result inflammation of the vocal folds.

More specifically to COVID-19, the vocal folds express a relatively high amount of ACE2 receptor, and infection by SARS-CoV-2 can lead to damaged vocal fold function. Because the ACE2 receptor also is expressed in muscles of the chest, lungs, and abdomen, muscles used to phonate may weaken, leading to voice issues such as dysphonia 1 . Cough also is a common symptom and can cause vocal fold trauma, and even mucosal tears or vocal fold hemorrhage. Additionally, patients with severe COVID-19 infection may require intubation.

Dysphonia and dysphagia after extubation are common 4 . In the cohort 1 , more females than males suffered from dysphonia, which could be due to sex-related differences in the inflammatory process although this is speculation, and further research is needed. There was a greater percentage of smokers among those with dysphonia compared to those without dysphonia. Additionally, those with dysphonia were more likely to have fatigue, chest pain, arthralgia, nausea, vomiting, diarrhea, cough, sputum that was sticky, and greater severity of dysphagia, nasal blockage, dyspnea, and ear, throat and face pain 1 . It is likely that dysphonia is under-reported due to more serious symptoms such as cough, respiratory distress at the time of presentation. It is also possible that cough caused by COVID-19 can lead to dysphonia from laryngeal damage. China, only 1 person (1.9%) had a sore throat 6 . As ORL symptoms become more prevalent than they were prior to COVID-19, there have been more ORL related Google searches. One study found that for ORL terms that were not medically technical, -Can't smell‖ saw the greatest increase in relative search volume (RSV), followed by -allergies,‖ -voice pain,‖ -ears ringing,‖ and -ear pain.‖ 7 Interestingly, the RSVs for -dysphagia,‖ -dysphonia,‖ and -thyroid nodule‖ all decreased. The study speculated that this could be because patients were not able to get their conditions evaluated by a physician, and that cancers possibly diagnosed less frequently as a result.

COVID-19 has potential long-term effects on singer and other professional voice users. COVID-19 can cause permanent lung damage. This lasting lung damage can cause mild-to-moderate reduction in pulmonary function (sometimes severe) that could be career-ending for professional voice users 8, 9, 10 . In a study of 150 patients who were followed up for sixty days after COVID-19, asthenia was reported in almost half of patients (74/150) at day thirty and 40% (52/130) at day 60. It was not determined whether dysphonia in each subject was due to neuropathy, vocal fold trauma from cough or intubation, malaise undermining vocal support, or some other cause 11 .

The principal mode by which people are infected with SARS-CoV-2 (is through exposure to respiratory aerosols or droplets carrying infectious virus. COVID-19 transmission can occur through contact transmission, droplet or aerosol transmission. Droplet transmission consists of exposure to larger droplets when a person is close to an infected person and airborne transmission consists of exposure to smaller droplets and particles at greater distances. COVID-19 particles also can last in the air for hours and on surfaces for days 12 . An aerosol is less than 5 µm in size, and a droplet is greater than 5 µm 13 . Sneezing, coughing and talking are well known mechanisms for transmitting aerosols and droplets [14] [15] [16] [17] [18] [19] [20] [21] [22] . J.P. Duguid characterized respiratory droplets by size and duration for bacteria. Sneezing and coughing were more likely to contain pathogens compared to normal talking. The smaller the size the bacteria, the longer it survived on surfaces 23 . A 1997 study from Papineni and Rosenthal demonstrated the size distribution of exhaled droplets from human subjects from mouth breathing, nose breathing, coughing and talking. They found that coughing produced the largest droplet concentrations, and nose breathing produced the smallest 24 Bahl et al used a respiratory droplet tracking apparatus to analyze whether certain syllables produced a greater aerosol/droplet velocity than others 29 . It found that respiratory droplets after -ti,‖ -fa,‖ and -do‖ were spoken had the same velocity (6 m/s) as respiratory droplets from usual speaking. Approximately 90% of droplets had a velocity of under 1 m/s and 75% had a velocity of under 0.5 m/s. Those that had a velocity greater than 1 m/s, tended to move between 120° and 240° from the mouth, while 75% of the droplets between 120° and 240° moved in all directions equally. Overall, the results found that greater amounts of aerosols were made during singing than repetitive speaking, and that the lower velocity droplets did not settle as quickly. In 2007, Yang et al characterized the size and concentration of respiratory droplets generated by a human cough. They found that the total average size distribution of the droplet nuclei was 0. 58-5.42 micron, and 82% of droplet nuclei were in 0.74-2.12 micron range 30 physiotherapy. They found that non-invasive ventilation and chest physiotherapy are droplet (not aerosol)-generating procedures, producing droplets of > 10 µm in size. They suggested that health care workers working within 1 m of an infected patient should use a high level of respiratory protection Nebulizers were found to produce small to medium size aerosols 33 .

Asymptomatic spread through aerosols has been documented 34 . A study from Hu et al demonstrated one of the first cases of asymptomatic spread in Germany 35 . Asymptomatic spread is a challenge for public health and has facilitated COVID-19 spread throughout the population 36 . This could increase risk for and from professional voice users.

Singing generates aerosols and droplets. In a 1968 study from Loudon and Roberts, singing increased the dissemination of tuberculosis compared to talking 37 . On April 29th, 2020, Germany set out rules for religious services including a ban on singing 38 . A study from Murbe et al demonstrated increase in particle emission during singing and emphasized the importance of risk management for singing 39 . A study by Reid looked at aerosol concentrations produced by speaking, singing and breathing. He found that speaking and singing showed steep increases in mass concentration with increase in volume (spanning a factor of 20-30 across the dynamic range measured, p<1×10-5). He found that at the quietest volume (50 to 60 dB), neither singing (p=0. 19) or speaking (p=0.20) was significantly different from breathing; however, at the loudest volume (90 to 100 dB), a statistically significant difference (p<1×10-5) was observed between singing and speaking, with singing generating a factor of between 1.5 and 3.4 more aerosol mass, further distinguishing the capability for aerosol production during singing 40 . There have been multiple choir events of also cited with COVID-19 outbreaks. On March 29 th , 2020, the LA Times reported on a choir that decided to hold practice during the beginning of the COVID-19 pandemic that led to the death of two members in Mount Vernon, Skagit County, Washington 41 . Following a 2.5-hour choir practice attended by 61 persons, including a symptomatic index patient, 32 confirmed and 20 probable secondary COVID-19 cases occurred (attack rate = 53.3% to 86.7%); three patients were hospitalized, and two died. They found that transmission was likely facilitated by close proximity (within 6 feet) during practice and augmented by the act of singing 42 . The COVID-19 pandemic might affect how large groups gather at events in the future, possibly long-term. This poses several problems, including how groups will sing together.

On May 18 th , 2020, the Philadelphia Inquirer released an article suggesting that choir singing would not be safe until the pandemic was under control 43 , but that comment was based on opinion, not evidence. In an NPR discussion, Is Singing Together Safe In The Era Of Coronavirus? Not Really, experts lay out the dangers of singing in a confined area, citing the dangers of aerosolization for both singers and wind instrumentalists 44 . Another article in the New York Times also cited the dangers of aerosolization for choirs also citing, the Performing Arts Aerosol study 45 . The Performing Arts Aerosol study, a study by scientists from the University of Colorado, Boulder and the University of Maryland, commissioned by a group of over 120 performing arts groups, looked at a clarinet, flute, horn, soprano singers, and trumpet aerosolization 46 . In their preliminary investigations, they found that concentrations were relatively higher for instruments that had straight shapes from mouthpiece to bell (trumpet, clarinet), and that masks and nylon bell coverings reduced particle concentrations. Based on their initial simulation they confirmed the effectiveness of social distancing directives to keep 6ft apart, as that is the boundary of the region around an infected person in which the risk of infection is high , especially with an exposure duration greater than 30 minutes 43 . They recommended that masks should be worn by all students and staff prior to entering a performing arts room. Masks should continue to be worn until all students are seated and ready for instruction and while talking. For instrument players, a small slit in the mask for the mouthpiece should be used while playing. In instrument groups where a mask physically be worn, the mask should be worn over the chin and replaced during periods during which the student is not 

Another harmful effect of the COVID-19 pandemic is psychological stress, which can affect the voice negatively 47, 48 . It is important to recognize the impact on the psychosocial stress of COVID-19 49, 50 and it is imperative that people engage in activities that are safe and stress relievers. The World Health Organization (WHO) released a document that addressed mental health and psychosocial considerations during the COVID-19 outbreak that encouraged regular routines and new routines that involved singing in one's own home 51 . Singing has the capability of bringing human beings closer together. In the initial outbreak in Italy on March 15 th , 2020, people quarantined in Italy joined in song and sang from their balconies to support first line workers 52 . One study examined how stress levels were associated with voice changes in a group of 313 Israeli professors as they switched to online teaching. The questionnaire allowed them to rate the severity of the following voice symptoms: fatigue, effort, weakening, throat soreness or pain, hoarseness, larynx dryness/irritation, the need to drink water often, and persistent throat clearing/coughing. Interestingly, those who had lower psychological stress before COVID-19 had a positive association between psychological stress and voice symptoms during the transition, and those who had higher psychological stress before COVID-19 had an even higher association 53 

Another voice complication from COVID-19 occurs in patients who have tracheoesophageal voice prostheses. Over time, these devices may lead to complications such as aspiration, which necessitate device replacement. Depending on circumstances, such as how severe the complication is and how far the patient is from an appropriate care facility, telemedicine may be used as a first approach due to the suspected high-risk of treating/replacing these devices. If the patient must come to the office, proper precautions must be taken and may include having the patient tested for COVID-19. If a patient is positive for COVID-19 but has a life-threatening complication from a tracheoesophageal prosthetic device, full precautions must be followed, including having the head and neck surgeon do both the medical assessment and the procedure in order to reduce the number of people who come in contact with the patient 55 . Another study examined similar protocols in patients with voice prosthesis. 37 of 73 patients could be contacted via telemedicine (50.68%). The problem could be resolved via telemedicine for 23 of the 37 patients (62.16%), whereas the 14 others had to visit the office. Patients who participated in telemedicine had significantly lower levels of depression and anxiety comparing before and after the telemedicine appointment. These patients also were satisfied overall with their telemedicine visits. It was concluded that for many patients, telemedicine can resolve issues and should be considered a viable option in the time of COVID-19 56 .

Because of the COVID-19 pandemic, ORL office practices have had to make substantial changes. All healthcare workers have been at risk of contracting COVID-19, but healthcare workers in ORL are at a higher risk of coming in contact with a patient's respiratory droplets or aerosols via cough, sputum, and a tracheotomy, for example, due to the nature of the body region. High risk procedures include video fluoroscopic swallowing exams and pharyngolaryngological endoscopy 57 . One perspective suggested primarily assessing the voice through clinical signs and reserving endoscopy for necessary instances 58 57 , and all patients should be examined using precautions that would be followed if a patient had known, active COVID-19. Telemedicine is an option for some ORL patients. One study of 125 patients found that there was an 87% satisfaction rate with the telemedicine appointments. Whether a patient was satisfied or not was found to not be based on their clinical conditions 60 . However, the senior author (RTS) has found telemedicine to be of limited value for the many dysphonia patients who require laryngeal examination by strobovideolaryngoscopy to establish an accurate diagnosis and safe voice use recommendations.

There has been focused effort on researching ways to diagnose COVID-19 more effectively. One research group has been creating a database, named Coswara, that collects sound data on both COVID-19 and healthy individuals. The four main categories of data collection were cough type, rate at which numbers 1 to 20 could be counted, breathing type, and how a constant vowel was phonated. Sound databases have been successful for other respiratory disorders such as tuberculosis, pneumonia, asthma, and pertussis; so, hopefully this approach will be successful for COVID-19, too 61 .

Voice and Speech Therapy COVID-19 has had an impact on voice and speech therapy. Sund et al studied a single subject and found that in voice production during voice assessment and therapy, there was an increase in respiratory particles compared to normal speech and baseline. Respiratory particle counts were higher at 15 cm compared to 1m from the particle sizer, suggesting that physical distance may reduce clinician exposure. In their study, the particles did not accumulate overtime 62 . Many voice therapy patients can have telemedicine sessions as can patients working with singing or acting voice specialists or teachers. This is a valuable modality, as it is estimated that 30% of people have a voice disorder, and this number is greater among professional voice users 63 . Statistically, some of these patients will be infected, perhaps without symptoms; and telemedicine will allow voice therapy and training to proceed safely for patients and providers. At this time, the patient should only have in-person sessions if necessary, with the understanding that there is a risk of spreading COVID-19. Semi-occluded voice therapy exercises (SOVTEs), such as speaking into a straw or tongue and lip trills, are popular voice exercises that cause the vocal tract to narrow, which can create turbulent and fast airflow and spread respiratory droplets easily 63, 64 . A protective measure is for the therapist and patient to both wearing masks. However, in this case, voice therapy sessions may be harder to conduct because the therapist may have difficulty demonstrating the exercises and the patient may have difficulty repeating them. Mask protection is also compromised when using a show. Voices may also be more difficult to hear on both sides, so the therapist may have difficulty concluding whether the patient performed the exercise correctly. However, if the patient and voice therapist decide to conduct an in-person session, precautions reduce the risks of spreading COVID-19 can be followed without substantially compromising the quality of the session 63 .

One study showed that there was greater airflow velocity in loud and whispered voices than in normal-volume voices use, consonants had greater airflow velocity than vowels, voice therapy exercises created lower airflow velocity than deep exhalation, and deep exhalation or constant vowel sound had a very high airflow velocity initially that decreased quickly. If these and other factors are understood and appropriate precautions are used, the risk of spreading COVID-19 can be minimized 64 . Another consideration is barriers to telemedicine voice therapy sessions. A study of Italian and French patients found that the four difficulties of telemedicine voice therapy were the lack of proper devices, such as cameras or software, not all voice therapists being confident in how to use technological devices the fact that elderly and poor patients may not have access to the required technology, and that the healthcare system and certain insurance companies do not pay for virtual voice therapy 63 . However, many studies have shown that telemedicine voice therapy is a viable alternative in a situation such as COVID-19. Many studies suggest that clinical outcomes from voice therapy via telemedicine are often not significantly different from those achieved when sessions were conducted in-person 65 . One study of telemedicine voice therapy for vocal fold nodule patients found that the patients had significantly improved clinical outcomes 66 . A similar conclusion was reached in a study with a cohort of muscle tension dysphonia patients 67 . Telemedicine voice therapy can be synchronous, in which the sessions can be performed in real-time, asynchronous, in which both the clinician and patient can upload/view materials at their own time such as videos or audio, and hybrid, which encompasses both synchronous and synchronous methods 68 . Voice therapy sessions should be provided in safe and practical ways for patients, whether the session is virtual or in-person; and patient therapy need not be interrupted because of the COVID-19 pandemic.

One interesting COVID-19 treatment option that has been proposed is hypertonic saline nasal irrigation and gargling (HSNIG). This was shown to decrease the time course of the COVID-19 upper respiratory tract infection by 1.9 days, transmission between people of the same household by 35%, usage of over-the-counter medication by 36%, and viral shedding 67 

The Wisconsin Council of Churches released a guideline on church music in the time of COVID-19. This council recommended using recorded music rather than live music; using piano, electronic keyboard, organ, stringed or percussion instruments rather than wind and brass instruments; having outdoor worship to allow for greater space for social distancing, improved ventilation and encouraging singing sacred music at home 72 . The American Choral Directors Association (ACDA) released a COVID-19 response committee report on June 15 th , 2020. The report was broken down into different age groups (middle school/junior high, senior high school, collegiate, community: youth and adult, and music in worship) and the teaching style (face-toface, hybrid and full remote). In general, they recommended reorganization into smaller groups to meet social distancing guidelines, wearing masks, having remote access for students with access to the internet, and using outdoor spaces when feasible. It is important to continue to make the social connections that are so significant in this age group 73 . The ACDA chose to prepare this document without medical or scientific input. Singing is possible with a mask but may cause breathing challenges for some, and this may affect especially singers with underlying pulmonary dysfunction. Voice fatigue is common but can be mitigated through voice therapy and/or training, finding a properly fit mask that allows for free movement of the jaw, and by taking voice breaks to rest and hydrate 74 .

The American Federation of Musicians (AFM) released a guideline for returning to work safety.

As with previously mentioned guidelines, the AFM reinforced the importance of the need for safety practices. For small-and-medium sized live venues, the AFM recommended keeping social distancing both onstage, and in the audience, no dancing, but use of the dance floor as a way to social distance from the audience, making sure one act leaves the stage completely before the next comes on, using virtual tip jars, and using drum shield-style Plexiglas in front of stage (singers) and between and/or in front of winds and brass. In the recording studio, it was recommended that winds and brass instrumentalists be separated when possible, congregation in the studio be avoided, musicians bring their own microphone and headphones, and that sanitization of equipment and surfaces be assured 75 . To return safely to the theatre, similar guidelines will apply including social distancing, mask wearing, health screenings, and avoiding shared equipment 76 . The National Association of Teachers of Singing put together a list of risk assessment tools that can be used to stratify the risk of COVID-19, transmission as well as guidelines like those previously mentioned 77 . The New York Times article, When Will it be Safe to Sing Together Again, pushed forth the pivotal question of when will be the right time?

The article mentions that in Norway, up to 50 people can sing together as long as everyone keeps 3 feet apart, while in Germany, the rules for group singing vary by region, with some regions spacing singers ten feet apart and other regions banning group singing. In the Netherlands, after more than 100 choristers became ill after a single concert in Amsterdam, group singing activities were strongly discouraged 78 . In order to return to music and theatre safely, it is important for musicians and professional voice users to follow social distancing, wear masks and follow COVID-19 guidelines.

Conclusion COVID-19 has had a major impact on singers and other musicians worldwide. It can of affect the voice and can lead to paresis/paralysis of laryngeal nerves to long-term changes in respiratory function. There is a risk from aerosolization/droplet formation transmission with singing, and with playing wind and brass instruments, that can be mitigated by following COVID-19 guidelines. Ways to reduce possible transmission during singing and instrument play include virtual rehearsals or performances, mask-wearing, instrument covers, smaller choirs, performing outside, excellent ventilation being socially-distanced, shorter rehearsals, regularly cleaning commonly-touched surfaces and washing hands, avoiding contact with others, and temperature screening.

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