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Airway reactivity-induced asthma in singers (Arias)
Journal of Voice
Vol. 5, No. 4, pp. 332-337 © 1991 Raven Press, Ltd., New York
Airway Reactivity-Induced Asthma in Singers (Arias) John R. Cohn, tRobert Thayer Sataloff, t Joseph R. Spiegel, *James E. Fish, and *Karen Kennedy Departments of*Medicine and ~Otolaryngology, Thomas Jefferson University, Philadelphia, Pennsylvania, U.S.A.
Summary: Professional singers are particularly attuned to changes in air flow that can alter their ability to perform. We describe four singers who complained primarily of performance-related vocalization problems, but who had normal larynges and fundamentally good voice technique. All had normal or near-normal spirometry. Subsequent studies revealed evidence of increased airway reactivity, either by response to bronchodilators or to methacholine. All responded to treatment with bronchodilators with improvement in vocal performance. This represents a form of airway reactivity-induced asthma in singers similar to that found with exercise or hyperventilation. Key Words: Singers--Asthma--Pulmonary disease--Obstructive pulmonary disease.
The phenomenon of exercise-induced asthma (EIA) has been recognized for many years (1). Subsequent clinical and experimental evidence has demonstrated that this syndrome is generally not a function of exercise itself, but rather represents changes in airway tone produced by exerciseinduced hyperventilation (2-5). Eucapneic hyperventilation of cold, dry air will cause bronchospasm in susceptible subjects. By contrast, patients with EIA may exercise for prolonged periods while inhaling air heated to 37 ° and fully saturated, without adverse effect on their flow rates (6). Singers, when they are performing, increase their minute ventilation, making them prone to the same kind of airway effects seen with other forms of exercise. As a group, professional performers may be particularly attuned to subtle changes in air flow. In phonation, the vocal folds act as an oscillator, producing a buzz-like sound. The quality of the sound is determined largely by the supraglottic vocal tract, which acts as a resonator, enhancing selected harmonics produced by the vocal folds. The power source of the voice is composed of the lungs, rib cage, abdomen, and back musculature. The combined actions of these structures create a vector of
force directing the air stream between the vocal folds, providing sufficient air pressure and flow to permit the complex adjustments in subglottal pressure necessary for speech and singing. The anatomic structures of the power source are collectively referred to by singers and actors as their "support." When singing technique is correct, adequate breath support permits modulation of pitch and loudness in an efficient fashion. When breath support is deficient, accessory muscles in the head and neck are brought into play. This inappropriate muscle use results in voice fatigue, decreased control (especially during soft singing), loss of range, and other vocal problems. Even slight changes in breath support may produce such problems under the rigorous physical demands of singing. Support may be undermined by improper muscle use (technique or neuromuscular pathology) or pulmonary dysfunction such as asthma. We describe four professional singers with demonstrated airway hyperreactivity who complained of voice fatigue or other voice problems while singing. All responded to bronchodilator therapy with improvement in their performance-related symptoms. Patients The four patients are professional singers who came for evaluation of voice dysfunction. They
Address correspondence and reprint requests to Dr. J. R. Cohn, Suite 4016, Thomas Jefferson University Hospital, 111 So. Eleventh St., Philadelphia, PA, 19107.
332
A I R W A Y REACTIVITY-INDUCED ASTHMA IN SINGERS
were selected for detailed pulmonary evaluation and treatment after specialized laryngologic examination revealed normal larynges and supraglottic structures, reasonably good vocal technique when rested, and complaints suggestive of lack of breath support, which was worse than apparent on examination. Each patient underwent complete history and physical examinations performed by a laryngologist and a pulmonologist. Particular attention was paid to the upper airway, larynx, and lower respiratory tract, including direct visualization of the larynx by strobovideolaryngoscopy. Each singer also underwent an extensive objective and subjective voice evaluation including laryngeal air flow testing, spectrography, acoustic analysis, phonatory function analysis, assessment by a speech-language pathologist, and evaluation by a singing voice specialist (7).
Pulmonary function testing Initial screening consisted of spirometry (S&M Instruments, Doylestown, PA, U.S.A.) using a dry rolling seal spirometer. The spirometer was interfaced to a personal computer (Samsung $550, Samsung Semiconductor & Telecommunications, San Jose, CA), which calculated standard measures of air flow and volume. Predicted values were determined based on each patient's age and height according to published equations (8). Methacholine challenge was performed according to standard techniques (9-11). Patients were initially given five breaths of methacholine (Roche, Nutley, N.J.) at a concentration of 0.025 mg/ml, using a dosimeter (S&M Instruments). Spirometry was repeated at 3 and 5 min after each dose was given. Doses were increased in a stepwise fashion until a patient received five inhalations of methacholine at a 25-mg/ml concentration or there was a 20% or greater fall in the FEV v The dose of methalcholine calculated to cause a 20% fall in forced expiratory volume (FEV) 1 was reported as the PD20FEV1. CASE REPORTS Case 1 A 32-year-old soprano had sung rock and roll professionally for approximately 8 years. She began studying singing approximately 2 years before she started performing rock music regularly. However, she stopped studying shortly after she began performing regularly. For several years she experienced intermittent hoarseness and was diagnosed as
333
having "vocal nodules" in January 1989. She resumed singing lessons with a classically trained voice teacher and underwent a 6-week course of therapy with a speech-language pathologist. Despite attempts to comply with her voice training, she had persistent problems with hoarseness, fatigue, loss of high range, pain while singing, and inability to sing softly. All of these problems were less troublesome at the beginning of a performance session. She sang 3-5 nights weekly. She also noted shortness of breath while singing during the year prior to evaluation. She was a lifetime nonsmoker and had no other health problems. Previous allergic evaluation revealed her to be atopic. She was unable to use any antihistamines because the mucosal drying interfered with her ability to sing. Otolaryngologic examination r e v e a l e d mild arytenoid erythema suggestive of reflux, and a small submucosal cyst on the right vocal fold, visible under stroboscopic light. Maximum phonation time and physiological frequency range were decreased, speaking fundamental frequency was excessively low, perturbation was elevated, s/z ratio was abnormal, and harmonic to noise ratio was abnormal (her singing and speaking technique revealed muscular tension dysphonia with deficient support and hyperfunction of neck and tongue muscles). She fatigued quickly and became short of breath during singing voice evaluation. Her chest was clear on auscultation. Baseline pulmonary function test results were normal, including a forced expiratory flow (FEF)zs_75 of 3.69 L/s (99% of predicted). Methacholine challenge was performed. The FEV~ fell to 21% after five breaths of methacholine at a concentration of 2.5 mg/ml. This resulted in a calculated PD2oFEV 1 of 11.9 units. The patient began sustained-released theophyUine (Slo-bid) therapy, 200 mg every 12 h. This resulted in a serum theophylline level of 11.1 mg/ml and was associated with an improvement in her symptoms. Her shortness of breath during performance, vocal fatigue, and ability to practice correct breath support improved quickly following medication. She was able to continue her performance requirements without fatigue or loss of range, and improved breath support resulted in voice quality good enough to obviate the need for surgical treatment of her submucosal cyst. Case 2 A 32-year-old professional singer and voice teacher described frequent colds as a child and Journal of Voice, Vol. 5, No. 4, 1991
334
J. R. C O H N E T A L .
chronic gastroesophageal reflux since college. Subsequently, she began to experience chest or throat tightness after smoke exposure. Four and a half months prior to her visit, she had a small cyst removed from her vocal cord. Three months before her visit, she began to notice night-time awakening with shortness of breath. This was subsequently found to be related to feather pillows and comforters, and her symptoms resolved when these were removed. Three to four weeks prior to her visiL she began to experience shortness of breath 15-30 min after starting to sing. She described this as a sensation of tightness in her chest. It would last up to 3 h. By contrast, she reported no difficuity with aerobics or walking out doors. She noted that she might walk 8-10 miles per day. Her only medication was ranitidine (Zantac), 150 mg twice daily. She had been involved in voice research projects, and extensive objective documentation of her voice and pulmonary function was available. Her recent complaints of shortness of breath were associated with decreased physiological and musical frequency range and increased inappropriate use of strap and tongue muscles (muscular tension dysphonia during performance). Strobovideolaryngoscopy revealed minimally decreased vibration in the vocal fold from which the cyst had been removed. Singing technique was initially good. However, after approximately 20 min of singing, tongue retraction and excessive strap muscle tension were obvious. Her lungs were clear to auscultation. Pulmonary function tests showed mild airway obstruction (Table 1). Following 20 min of singing, there was a small, statistically insignificant decrease in her FEV1 from 2.97 to 2.89 L. A methacholine challenge was performed. This was negative with a small decrease in FEV ~noted at a 25-mg/ml dose. There was no change in her midexpiratory flow rate. Albuterol, 2.5 mg, was administered by high-flow nebulizer. The FEV~ increased TABLE 1. Pulmonary function of case 2 before and after treatment with albuterol, 2.5 mg, by high flow nebulizer
FVC, (L) FEV1, (L) FEF25_75, (L/s) PEFR, (L/s)
Pretreatment
Posttreatment
% change
3.78 2.68 1.96 7.35
3.74 3.05 2.91 6.98
- 2 + 12 +24 - 5
FVC, forced vital capacity; FEV, forced expiratory volume; FEF, forced expiratory flow; PEFR, peak expiratory flow rate. Journal of Voice, Vol. 5, No. 4, 1991
from a baseline of 2.68 to 3.05 L, representing a 14% increase, and her FEFzs_75 increased 35% from 2.16 to 2.91 L/s (Table 1). She was advised to use albuterol, two puffs by metered-dose inhaler, before singing. This resulted in immediate and definite improvement in her symptoms, confirmed by objective voice measures. When she stopped using the albuterol, her symptoms returned. They disappeared promptly when albuterol was resumed. Case 3
A 32-year-old mezzo soprano and a singing teacher was a Metropolitan Opera audition winner. She reported a history of mild allergic rhinitis and asthma when she was in her mid-20s. She was treated with allergy vaccine with minimal subsequent symptoms. She had used no asthma medication in the previous 4 years. She reported no voice difficulties until her 8th month of pregnancy, about 5 months prior to her laryngologic evaluation. At that time, she noted voice fatigue, and unusual voice break, and loss of range. These problems persisted following delivery by cesarean section. She also complained of marked reflux symptoms. In addition, she had a history of vocal fold hemorrhage that occurred during an acute asthma attack on an airplane 3 years prior to her pregnancy. Strobovideolaryngoscopy revealed a varicosity of her left vocal fold that did not interfere with phonation, and signs of gastroesophageal reflux laryngitis. Singing examination revealed ineffective support with increased jaw, neck, and tongue muscle tension. Similar abuses were present during speaking, but to a lesser degree. Objective analysis revealed decreased maximum phonation time. Her chest was clear to auscultation. Spirometry was normal, with an FEF25_75 of 3.91 L/s (104% of predicted). Methacholine challenge resulted in a 21% fall in her FEV1 after five breaths of methacholine, at a concentration of 2.5 mg/ml. Her calculated PD2oFEV 1 was 12.7 units. Albuterol, two puffs prior to singing, was prescribed. This improved her symptoms substantially, although not completely. She was also treated with a strict antireflux regimen and intensive speaking and singing therapy. Her phonation time, range, and fatigue improved significantly within 1 week, allowing her to resume vocal study safely. Case 4
A 28-year-old professional opera singer denied having any unusual respiratory problems until age 22. At that time, she began to have some pollen-
A I R W A Y REACTIVITY-INDUCED ASTHMA IN SINGERS
related upper respiratory symptoms while living in New Mexico. She was well when she lived in Houston. She moved to Philadelphia in September to begin additional voice training. Routine evaluation at that time revealed difficulty singing in her lower register. She was unable to maintain effective support, particularly after prolonged periods of singing. Strobovideolaryngoscopy was normal. Her singing technique was good at rest, and her objective voice measures were within normal limits. However, they were not as good as might be expected for her level of training. Her lungs were clear. Baseline FEV~ was 2.47 L (70% of predicted). Following the inhalation of two puffs of albuterol from a metered-dose inhaler, she had a 16% increase in her FEV1, to 2.86 L. Her midflow was similarly increased (Table 2). Albuterol, two puffs before singing, was prescribed. She noted considerable improvement, reporting that she was "singing better than ever." A sustained-released albuterol tablet (Proventil Repetabs) was prescribed. This resulted in additional improvement. She continued to supplement the oral beta agonist with a metered-dose inhaler as needed. SUMMARY OF RESULTS The patients with airway reactivity-induced asthma in singers (ARIAS) consisted of four women with a mean age of 31.3 years (Table 3). There were no smokers in the group. All four patients gave a history of allergic respiratory problems in the past. Two underwent prick allergen skin testing but only one had a positive response. There were three classical singers, including one professional voice instructor, and one popular music singer. Two patients had completely normal baseline spirometry, while two patients had mild airway obstruction. None was symptomatic except when singing. The two patients with normal pulmonary function tests underwent methacholine challenge, with an average PD2oFEV1 of 12.3 breath units. The third patient, TABLE 2. Pulmonary function o f case 4 before and
after treatment with albuterol, 2.5 rag, by high-flow nebulizer % FVC, (L) FEVI, (L) FEF25_75, (L/s) PEFR, (L/s)
Pretreatment
Posttreatment
change
3.68 2.47 1.62 6.44
3.87 2.86 2.21 7.54
5 16 37 17
FVC, forced vital capacity; FEV, forced expiratory volume; FEF, forced expiratory flow; PEFR, peak expiratory flow rate.
335
T A B L E 3. Initial pulmonary function and treatment o f
patients with A R I A S Baseline, % predicted Patient
FEV 1
1
102
FEF25_75 PD2oFEVI 103
2
88
50
Negative
3
101
94
4
70
12.7 • Not done
11.9
Treatment Slo-bid, 200 mg, 1-12 h Albuterol, 2 puffs before singing Albuterol, 2 puffs before singing Oral and inhaled albuterol
ARIAS, airway reactivity-induced asthma in singers. PD2o FEV~, provocative dose at which 20% in FEV~.
who had mild airway obstruction on baseline testing, had only a 2% fall in FEV1 after receiving a dose of 169 breath units of methacholine. She was then given albuterol, 2.5 mg by high-flow nebulizer, with a 14% increase in her FEV1 and a 35% increase in her FEF25_75. The fourth patient had a 16% increase following bronchodilator in her FEV1 on initial testing. Patients were treated with a variety of medications, depending on their circumstances. Two patients were instructed to use albuterol by metereddose inhaler before singing, one was given a sustained release form of albuterol (Proventil Repetabs), supplemented with a metered-dose inhaler, and the fourth was given sustained-released theophylline only. All reported improvement in vocal endurance and quality, without adverse effect. DISCUSSION The mechanism involved in vocalization has been studied carefully (12). Efficient support is essential to healthy speaking and singing (13). When abnormalities of muscle or lung function interfere with breath support, voice symptoms are common, and serious vocal pathologic conditions (such as nodules and cysts) may ensue. Professional singers are particularly attuned to subtle changes in air flow and pressure. Professional singers are the Olympic athletes of voice users. Because of the great physical demands of singing, even slight changes in physical ability may be immediately obvious and potentially disabling. Such problems may also be encountered among professional speakers including not only actors, but also clergy, politicians, trial attorneys, and others. Speakers and amateur singers are somewhat less inclined to seek medical attention for minor voice disturbances. So it is incumJournal of Voice, Vol. 5, No. 4, 1991
336
J. R. C O H N E T A L .
bent on physicians to remain alert for these problems. There was no single unifying complaint experienced by all of our patients. While two identified dyspnea after performing or practicing for prolonged periods, the others noted disturbances with the quality or endurance of their singing voices. It is not uncommon to see patients who have difficulty characterizing the source of chest discomfort (14), and so the variable initial appearance of our patients should not present a problem in linking their heterogeneous complaints to an airway disorder. All of our subjects were found to have normal upper airways. All but one (case 2) had tried a variety of empiric treatments without benefit, casting doubt on the likelihood of a placebo effect accounting for their improvement. Our patients demonstrated increased airway reactivity, either by their response to methacholine or to an inhaled bronchodilator. An attempt was made in two instances to demonstrate a change in expiratory flow rates after singing, but they were not able to duplicate their problems in the office. This may have reflected a reduced respiratory effort when practicing in an unusual environment. Alternatively, they may have been more sensitive to subtle changes in their respiratory system than could be detected with conventional spirometry. Unfortunately, body plethysmography was not available at the time of clinical evaluation. Experimental laboratory evidence has demonstrated that EIA is temperature and humidity related. Patients with EIA may exercise using humidified warm air without difficulty. By contrast, hyperventilation of cold, dry air rapidly provokes a response (3). This appears to be secondary to increased airway drying from cold, dry air. The upper respiratory tract is responsible for warming and humidifying air. Increased air flow with exercise, as well as the tendency toward mouth breathing with increased ventilation, impairs these protective mechanisms. Singers do a considerable amount of mouth breathing when performing, making them susceptible to the same kinds of problems, They also practice and perform in environments over which they have no control and that are often unfavorable. Our patients have been treated with a variety of medications. Initial treatment has generally consisted of a sympathomimetic inhaler. While concerns could be raised about the effect of a smooth muscle relaxant on vocal cord function (15), we Journal of Voice, Vol. 5, No. 4, 1991
have not experienced complaints with limited use of this type of medication. Some patients may have mild laryngitis from inhaled medications or propellants. Inhalant medications must be used with caution, especially preceding a performance. The effect of inhaled corticosteroids on the smooth muscle of the vocal cord is uncertain, although vocal cord dysfunction has been observed with long-term exposure to inhaled corticosteroids (15,16). Similarly, oral bronchodilators decrease lower esophageal sphincter tone (17,18) creating the potential for exacerbation of gastroesophageal reflux, another problem in this population (19). Oral bronchodilators may also cause a slight tremor that is audible during soft singing in some cases. Allergy evaluation and treatment are ideally suited to singers with atopic problems (20). Unlike the medications listed, they has no adverse effects on the vocal apparatus. Careful, individualized adjustment of medications is essential for each professional voice user. In summary, singers who complain of problems with voice quality, range, or endurance and who are without a readily apparent abnormality of the larynx or singing technique should have pulmonary evaluation. If routine pulmonary function test resuits are abnormal, their response to bronchodilators should be measured. If they are normal, methacholine challenge should be performed to evaluate them for the possibility of ARIAS. Patients with ARIAS appear to respond well to the same medications used to treat other forms of ventilationinduced bronchospasm, although physicians must be alert for "minor" medication side effects that may impair performance. The ARIAS requires further investigation. It is hoped that this preliminary report will lead to controlled studies to clarify the nature of this entity and its optimal treatment. Acknowledgment:The authors want to thank Reva Silver for her secretarial assistance with the preparation of this manuscript, and Mary Hawkshaw, R.N., B.S.N., for her editorial assistance. REFERENCES 1. Haynes RL, Ingram RH Jr., McFadden ER Jr. An assessment of the pulmonary response to exercise in asthma and an analysis of the factors influencing it. A m R e v Respir Dis 1976;114:739--42. 2. Strauss RH, McFadden ER Jr, Ingram RH Jr, Jaeger JJ. Enhancement of exercise-induced asthma by cold air. N Engl J M e d 1977;297:743-7. 3. Deal EC J, McFadden ER Jr, Ingrain RH Jr, Jaeger JJ. In-
A I R W A Y REACTIVITY-INDUCED ASTHMA IN SINGERS
4. 5. 6. 7. 8. 9.
10.
11.
fluence of heat and humidity on the airway obstruction induced by exercise in asthma. J Clin Invest 1978;61:433-40. Deal EC J, McFadden ER Jr, Ingrain RH Jr, Jaeger JJ. Hyperpnea and heat flux: initial reaction sequence in exerciseinduced asthma. J Appl Physiol 1979;46:476--83. McFadden ER Jr, Ingram RH Jr. Exercise induced asthma: observations on the initiating stimulus. N Engl J M e d 1979;301:763-9. McFadden ER Jr, !ngram RH Jr, Strauss RH, Jaeger JJ. Role of respiratory heat exchange in production of exerciseinduced asthma. J Appl Physiol 1979;46:467-75. SataloffRT, Spiegel JR, Carroll LM, Darby KS, Hawkshaw M, Rulnick RK. The clinical voice laboratory: clinical application. J Voice 1990;4:264-279. Crapo RO, Morris AH, Gardner RM. Reference spirometric values using techniques and equipment that meet ATS recommendations. A m Rev Respir Dis 1981;123:659-64. Cartier A, Berustein IL, Burge PS, Cohn JR. Guideltnes for bronchoprovocation on the investion of occupational asthma: report of the subcommittee on bronchoprovocation for occupational asthma. J Allergy Clin Immunol 1989;84: 823-9. Fish JE, Rosenthal RR, Batra G, Menkes H, Summer W, Permutt S, Norman P. Airway responses to methacholine in allergic and nonallergic subjects. A m Rev Respir Dis 1976; 113:579-86. Ryan G, Dolovich MB, Roberts RS, Frith PA, Juniper EF, Hargreave FE, Newhouse MT. Standardization of inhala-
12. 13. 14. 15.
16. 17. 18. 19. 20.
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tion provocation tests: two techniques of aerosol generation and inhalation compared. A m Rev Respir Dis 1981;123: 195-9. Sundberg J. Science o f the singing voice. DeKalb: Northern Illinois University Press, 1987. Sataloff RT. Professional voice: the science and art o f clinical care. New York: Raven Press, 1991. Murray JF. Respiratory Diseases. In: Wyngaarden JB, Smith LH, eds. Textbook o f medicine. Philadelphia: WB Saunders, 1988:390--4. Williams AJ, Baghat MS, Stableforth DE, Cayton RM, Shenoi PM, Skinner C. Dysphonia caused by inhaled steroids: recognition of a characteristic laryngeal abnormality. Thorax 1983;38:813-21. Check WA, Kaliner MA. Pharmacology" and pharmacokinetits of topical corticosteroid derivatives used for asthma therapy. A m Rev Respir Dis 1990;141:844-51. Olson NR. Effects of stomach acid on the larynx. Proc A m Laryngol Assoc 1983;104:108-12. Richter JE, Castell DO. Drugs, foods and other substances in the cause and treatment of reflux esophagitis. M e d Clin North A m 1981;65:1223-34. SataloffRT. The professional voice, part II1. Common diagnoses and treatments. J Voice 1987;1:283-92. Spiegel JR, Sataloff RT, Cohn JR, Hawkshaw M. Respiratory function in singers: medical assessment, diagnoses and treatments. J Voice 1988;2:40-50.
Journal of Voice, Vol. 5, No. 4, 1991
Vol. 5, No. 4, pp. 332-337 © 1991 Raven Press, Ltd., New York
Airway Reactivity-Induced Asthma in Singers (Arias) John R. Cohn, tRobert Thayer Sataloff, t Joseph R. Spiegel, *James E. Fish, and *Karen Kennedy Departments of*Medicine and ~Otolaryngology, Thomas Jefferson University, Philadelphia, Pennsylvania, U.S.A.
Summary: Professional singers are particularly attuned to changes in air flow that can alter their ability to perform. We describe four singers who complained primarily of performance-related vocalization problems, but who had normal larynges and fundamentally good voice technique. All had normal or near-normal spirometry. Subsequent studies revealed evidence of increased airway reactivity, either by response to bronchodilators or to methacholine. All responded to treatment with bronchodilators with improvement in vocal performance. This represents a form of airway reactivity-induced asthma in singers similar to that found with exercise or hyperventilation. Key Words: Singers--Asthma--Pulmonary disease--Obstructive pulmonary disease.
The phenomenon of exercise-induced asthma (EIA) has been recognized for many years (1). Subsequent clinical and experimental evidence has demonstrated that this syndrome is generally not a function of exercise itself, but rather represents changes in airway tone produced by exerciseinduced hyperventilation (2-5). Eucapneic hyperventilation of cold, dry air will cause bronchospasm in susceptible subjects. By contrast, patients with EIA may exercise for prolonged periods while inhaling air heated to 37 ° and fully saturated, without adverse effect on their flow rates (6). Singers, when they are performing, increase their minute ventilation, making them prone to the same kind of airway effects seen with other forms of exercise. As a group, professional performers may be particularly attuned to subtle changes in air flow. In phonation, the vocal folds act as an oscillator, producing a buzz-like sound. The quality of the sound is determined largely by the supraglottic vocal tract, which acts as a resonator, enhancing selected harmonics produced by the vocal folds. The power source of the voice is composed of the lungs, rib cage, abdomen, and back musculature. The combined actions of these structures create a vector of
force directing the air stream between the vocal folds, providing sufficient air pressure and flow to permit the complex adjustments in subglottal pressure necessary for speech and singing. The anatomic structures of the power source are collectively referred to by singers and actors as their "support." When singing technique is correct, adequate breath support permits modulation of pitch and loudness in an efficient fashion. When breath support is deficient, accessory muscles in the head and neck are brought into play. This inappropriate muscle use results in voice fatigue, decreased control (especially during soft singing), loss of range, and other vocal problems. Even slight changes in breath support may produce such problems under the rigorous physical demands of singing. Support may be undermined by improper muscle use (technique or neuromuscular pathology) or pulmonary dysfunction such as asthma. We describe four professional singers with demonstrated airway hyperreactivity who complained of voice fatigue or other voice problems while singing. All responded to bronchodilator therapy with improvement in their performance-related symptoms. Patients The four patients are professional singers who came for evaluation of voice dysfunction. They
Address correspondence and reprint requests to Dr. J. R. Cohn, Suite 4016, Thomas Jefferson University Hospital, 111 So. Eleventh St., Philadelphia, PA, 19107.
332
A I R W A Y REACTIVITY-INDUCED ASTHMA IN SINGERS
were selected for detailed pulmonary evaluation and treatment after specialized laryngologic examination revealed normal larynges and supraglottic structures, reasonably good vocal technique when rested, and complaints suggestive of lack of breath support, which was worse than apparent on examination. Each patient underwent complete history and physical examinations performed by a laryngologist and a pulmonologist. Particular attention was paid to the upper airway, larynx, and lower respiratory tract, including direct visualization of the larynx by strobovideolaryngoscopy. Each singer also underwent an extensive objective and subjective voice evaluation including laryngeal air flow testing, spectrography, acoustic analysis, phonatory function analysis, assessment by a speech-language pathologist, and evaluation by a singing voice specialist (7).
Pulmonary function testing Initial screening consisted of spirometry (S&M Instruments, Doylestown, PA, U.S.A.) using a dry rolling seal spirometer. The spirometer was interfaced to a personal computer (Samsung $550, Samsung Semiconductor & Telecommunications, San Jose, CA), which calculated standard measures of air flow and volume. Predicted values were determined based on each patient's age and height according to published equations (8). Methacholine challenge was performed according to standard techniques (9-11). Patients were initially given five breaths of methacholine (Roche, Nutley, N.J.) at a concentration of 0.025 mg/ml, using a dosimeter (S&M Instruments). Spirometry was repeated at 3 and 5 min after each dose was given. Doses were increased in a stepwise fashion until a patient received five inhalations of methacholine at a 25-mg/ml concentration or there was a 20% or greater fall in the FEV v The dose of methalcholine calculated to cause a 20% fall in forced expiratory volume (FEV) 1 was reported as the PD20FEV1. CASE REPORTS Case 1 A 32-year-old soprano had sung rock and roll professionally for approximately 8 years. She began studying singing approximately 2 years before she started performing rock music regularly. However, she stopped studying shortly after she began performing regularly. For several years she experienced intermittent hoarseness and was diagnosed as
333
having "vocal nodules" in January 1989. She resumed singing lessons with a classically trained voice teacher and underwent a 6-week course of therapy with a speech-language pathologist. Despite attempts to comply with her voice training, she had persistent problems with hoarseness, fatigue, loss of high range, pain while singing, and inability to sing softly. All of these problems were less troublesome at the beginning of a performance session. She sang 3-5 nights weekly. She also noted shortness of breath while singing during the year prior to evaluation. She was a lifetime nonsmoker and had no other health problems. Previous allergic evaluation revealed her to be atopic. She was unable to use any antihistamines because the mucosal drying interfered with her ability to sing. Otolaryngologic examination r e v e a l e d mild arytenoid erythema suggestive of reflux, and a small submucosal cyst on the right vocal fold, visible under stroboscopic light. Maximum phonation time and physiological frequency range were decreased, speaking fundamental frequency was excessively low, perturbation was elevated, s/z ratio was abnormal, and harmonic to noise ratio was abnormal (her singing and speaking technique revealed muscular tension dysphonia with deficient support and hyperfunction of neck and tongue muscles). She fatigued quickly and became short of breath during singing voice evaluation. Her chest was clear on auscultation. Baseline pulmonary function test results were normal, including a forced expiratory flow (FEF)zs_75 of 3.69 L/s (99% of predicted). Methacholine challenge was performed. The FEV~ fell to 21% after five breaths of methacholine at a concentration of 2.5 mg/ml. This resulted in a calculated PD2oFEV 1 of 11.9 units. The patient began sustained-released theophyUine (Slo-bid) therapy, 200 mg every 12 h. This resulted in a serum theophylline level of 11.1 mg/ml and was associated with an improvement in her symptoms. Her shortness of breath during performance, vocal fatigue, and ability to practice correct breath support improved quickly following medication. She was able to continue her performance requirements without fatigue or loss of range, and improved breath support resulted in voice quality good enough to obviate the need for surgical treatment of her submucosal cyst. Case 2 A 32-year-old professional singer and voice teacher described frequent colds as a child and Journal of Voice, Vol. 5, No. 4, 1991
334
J. R. C O H N E T A L .
chronic gastroesophageal reflux since college. Subsequently, she began to experience chest or throat tightness after smoke exposure. Four and a half months prior to her visit, she had a small cyst removed from her vocal cord. Three months before her visit, she began to notice night-time awakening with shortness of breath. This was subsequently found to be related to feather pillows and comforters, and her symptoms resolved when these were removed. Three to four weeks prior to her visiL she began to experience shortness of breath 15-30 min after starting to sing. She described this as a sensation of tightness in her chest. It would last up to 3 h. By contrast, she reported no difficuity with aerobics or walking out doors. She noted that she might walk 8-10 miles per day. Her only medication was ranitidine (Zantac), 150 mg twice daily. She had been involved in voice research projects, and extensive objective documentation of her voice and pulmonary function was available. Her recent complaints of shortness of breath were associated with decreased physiological and musical frequency range and increased inappropriate use of strap and tongue muscles (muscular tension dysphonia during performance). Strobovideolaryngoscopy revealed minimally decreased vibration in the vocal fold from which the cyst had been removed. Singing technique was initially good. However, after approximately 20 min of singing, tongue retraction and excessive strap muscle tension were obvious. Her lungs were clear to auscultation. Pulmonary function tests showed mild airway obstruction (Table 1). Following 20 min of singing, there was a small, statistically insignificant decrease in her FEV1 from 2.97 to 2.89 L. A methacholine challenge was performed. This was negative with a small decrease in FEV ~noted at a 25-mg/ml dose. There was no change in her midexpiratory flow rate. Albuterol, 2.5 mg, was administered by high-flow nebulizer. The FEV~ increased TABLE 1. Pulmonary function of case 2 before and after treatment with albuterol, 2.5 mg, by high flow nebulizer
FVC, (L) FEV1, (L) FEF25_75, (L/s) PEFR, (L/s)
Pretreatment
Posttreatment
% change
3.78 2.68 1.96 7.35
3.74 3.05 2.91 6.98
- 2 + 12 +24 - 5
FVC, forced vital capacity; FEV, forced expiratory volume; FEF, forced expiratory flow; PEFR, peak expiratory flow rate. Journal of Voice, Vol. 5, No. 4, 1991
from a baseline of 2.68 to 3.05 L, representing a 14% increase, and her FEFzs_75 increased 35% from 2.16 to 2.91 L/s (Table 1). She was advised to use albuterol, two puffs by metered-dose inhaler, before singing. This resulted in immediate and definite improvement in her symptoms, confirmed by objective voice measures. When she stopped using the albuterol, her symptoms returned. They disappeared promptly when albuterol was resumed. Case 3
A 32-year-old mezzo soprano and a singing teacher was a Metropolitan Opera audition winner. She reported a history of mild allergic rhinitis and asthma when she was in her mid-20s. She was treated with allergy vaccine with minimal subsequent symptoms. She had used no asthma medication in the previous 4 years. She reported no voice difficulties until her 8th month of pregnancy, about 5 months prior to her laryngologic evaluation. At that time, she noted voice fatigue, and unusual voice break, and loss of range. These problems persisted following delivery by cesarean section. She also complained of marked reflux symptoms. In addition, she had a history of vocal fold hemorrhage that occurred during an acute asthma attack on an airplane 3 years prior to her pregnancy. Strobovideolaryngoscopy revealed a varicosity of her left vocal fold that did not interfere with phonation, and signs of gastroesophageal reflux laryngitis. Singing examination revealed ineffective support with increased jaw, neck, and tongue muscle tension. Similar abuses were present during speaking, but to a lesser degree. Objective analysis revealed decreased maximum phonation time. Her chest was clear to auscultation. Spirometry was normal, with an FEF25_75 of 3.91 L/s (104% of predicted). Methacholine challenge resulted in a 21% fall in her FEV1 after five breaths of methacholine, at a concentration of 2.5 mg/ml. Her calculated PD2oFEV 1 was 12.7 units. Albuterol, two puffs prior to singing, was prescribed. This improved her symptoms substantially, although not completely. She was also treated with a strict antireflux regimen and intensive speaking and singing therapy. Her phonation time, range, and fatigue improved significantly within 1 week, allowing her to resume vocal study safely. Case 4
A 28-year-old professional opera singer denied having any unusual respiratory problems until age 22. At that time, she began to have some pollen-
A I R W A Y REACTIVITY-INDUCED ASTHMA IN SINGERS
related upper respiratory symptoms while living in New Mexico. She was well when she lived in Houston. She moved to Philadelphia in September to begin additional voice training. Routine evaluation at that time revealed difficulty singing in her lower register. She was unable to maintain effective support, particularly after prolonged periods of singing. Strobovideolaryngoscopy was normal. Her singing technique was good at rest, and her objective voice measures were within normal limits. However, they were not as good as might be expected for her level of training. Her lungs were clear. Baseline FEV~ was 2.47 L (70% of predicted). Following the inhalation of two puffs of albuterol from a metered-dose inhaler, she had a 16% increase in her FEV1, to 2.86 L. Her midflow was similarly increased (Table 2). Albuterol, two puffs before singing, was prescribed. She noted considerable improvement, reporting that she was "singing better than ever." A sustained-released albuterol tablet (Proventil Repetabs) was prescribed. This resulted in additional improvement. She continued to supplement the oral beta agonist with a metered-dose inhaler as needed. SUMMARY OF RESULTS The patients with airway reactivity-induced asthma in singers (ARIAS) consisted of four women with a mean age of 31.3 years (Table 3). There were no smokers in the group. All four patients gave a history of allergic respiratory problems in the past. Two underwent prick allergen skin testing but only one had a positive response. There were three classical singers, including one professional voice instructor, and one popular music singer. Two patients had completely normal baseline spirometry, while two patients had mild airway obstruction. None was symptomatic except when singing. The two patients with normal pulmonary function tests underwent methacholine challenge, with an average PD2oFEV1 of 12.3 breath units. The third patient, TABLE 2. Pulmonary function o f case 4 before and
after treatment with albuterol, 2.5 rag, by high-flow nebulizer % FVC, (L) FEVI, (L) FEF25_75, (L/s) PEFR, (L/s)
Pretreatment
Posttreatment
change
3.68 2.47 1.62 6.44
3.87 2.86 2.21 7.54
5 16 37 17
FVC, forced vital capacity; FEV, forced expiratory volume; FEF, forced expiratory flow; PEFR, peak expiratory flow rate.
335
T A B L E 3. Initial pulmonary function and treatment o f
patients with A R I A S Baseline, % predicted Patient
FEV 1
1
102
FEF25_75 PD2oFEVI 103
2
88
50
Negative
3
101
94
4
70
12.7 • Not done
11.9
Treatment Slo-bid, 200 mg, 1-12 h Albuterol, 2 puffs before singing Albuterol, 2 puffs before singing Oral and inhaled albuterol
ARIAS, airway reactivity-induced asthma in singers. PD2o FEV~, provocative dose at which 20% in FEV~.
who had mild airway obstruction on baseline testing, had only a 2% fall in FEV1 after receiving a dose of 169 breath units of methacholine. She was then given albuterol, 2.5 mg by high-flow nebulizer, with a 14% increase in her FEV1 and a 35% increase in her FEF25_75. The fourth patient had a 16% increase following bronchodilator in her FEV1 on initial testing. Patients were treated with a variety of medications, depending on their circumstances. Two patients were instructed to use albuterol by metereddose inhaler before singing, one was given a sustained release form of albuterol (Proventil Repetabs), supplemented with a metered-dose inhaler, and the fourth was given sustained-released theophylline only. All reported improvement in vocal endurance and quality, without adverse effect. DISCUSSION The mechanism involved in vocalization has been studied carefully (12). Efficient support is essential to healthy speaking and singing (13). When abnormalities of muscle or lung function interfere with breath support, voice symptoms are common, and serious vocal pathologic conditions (such as nodules and cysts) may ensue. Professional singers are particularly attuned to subtle changes in air flow and pressure. Professional singers are the Olympic athletes of voice users. Because of the great physical demands of singing, even slight changes in physical ability may be immediately obvious and potentially disabling. Such problems may also be encountered among professional speakers including not only actors, but also clergy, politicians, trial attorneys, and others. Speakers and amateur singers are somewhat less inclined to seek medical attention for minor voice disturbances. So it is incumJournal of Voice, Vol. 5, No. 4, 1991
336
J. R. C O H N E T A L .
bent on physicians to remain alert for these problems. There was no single unifying complaint experienced by all of our patients. While two identified dyspnea after performing or practicing for prolonged periods, the others noted disturbances with the quality or endurance of their singing voices. It is not uncommon to see patients who have difficulty characterizing the source of chest discomfort (14), and so the variable initial appearance of our patients should not present a problem in linking their heterogeneous complaints to an airway disorder. All of our subjects were found to have normal upper airways. All but one (case 2) had tried a variety of empiric treatments without benefit, casting doubt on the likelihood of a placebo effect accounting for their improvement. Our patients demonstrated increased airway reactivity, either by their response to methacholine or to an inhaled bronchodilator. An attempt was made in two instances to demonstrate a change in expiratory flow rates after singing, but they were not able to duplicate their problems in the office. This may have reflected a reduced respiratory effort when practicing in an unusual environment. Alternatively, they may have been more sensitive to subtle changes in their respiratory system than could be detected with conventional spirometry. Unfortunately, body plethysmography was not available at the time of clinical evaluation. Experimental laboratory evidence has demonstrated that EIA is temperature and humidity related. Patients with EIA may exercise using humidified warm air without difficulty. By contrast, hyperventilation of cold, dry air rapidly provokes a response (3). This appears to be secondary to increased airway drying from cold, dry air. The upper respiratory tract is responsible for warming and humidifying air. Increased air flow with exercise, as well as the tendency toward mouth breathing with increased ventilation, impairs these protective mechanisms. Singers do a considerable amount of mouth breathing when performing, making them susceptible to the same kinds of problems, They also practice and perform in environments over which they have no control and that are often unfavorable. Our patients have been treated with a variety of medications. Initial treatment has generally consisted of a sympathomimetic inhaler. While concerns could be raised about the effect of a smooth muscle relaxant on vocal cord function (15), we Journal of Voice, Vol. 5, No. 4, 1991
have not experienced complaints with limited use of this type of medication. Some patients may have mild laryngitis from inhaled medications or propellants. Inhalant medications must be used with caution, especially preceding a performance. The effect of inhaled corticosteroids on the smooth muscle of the vocal cord is uncertain, although vocal cord dysfunction has been observed with long-term exposure to inhaled corticosteroids (15,16). Similarly, oral bronchodilators decrease lower esophageal sphincter tone (17,18) creating the potential for exacerbation of gastroesophageal reflux, another problem in this population (19). Oral bronchodilators may also cause a slight tremor that is audible during soft singing in some cases. Allergy evaluation and treatment are ideally suited to singers with atopic problems (20). Unlike the medications listed, they has no adverse effects on the vocal apparatus. Careful, individualized adjustment of medications is essential for each professional voice user. In summary, singers who complain of problems with voice quality, range, or endurance and who are without a readily apparent abnormality of the larynx or singing technique should have pulmonary evaluation. If routine pulmonary function test resuits are abnormal, their response to bronchodilators should be measured. If they are normal, methacholine challenge should be performed to evaluate them for the possibility of ARIAS. Patients with ARIAS appear to respond well to the same medications used to treat other forms of ventilationinduced bronchospasm, although physicians must be alert for "minor" medication side effects that may impair performance. The ARIAS requires further investigation. It is hoped that this preliminary report will lead to controlled studies to clarify the nature of this entity and its optimal treatment. Acknowledgment:The authors want to thank Reva Silver for her secretarial assistance with the preparation of this manuscript, and Mary Hawkshaw, R.N., B.S.N., for her editorial assistance. REFERENCES 1. Haynes RL, Ingram RH Jr., McFadden ER Jr. An assessment of the pulmonary response to exercise in asthma and an analysis of the factors influencing it. A m R e v Respir Dis 1976;114:739--42. 2. Strauss RH, McFadden ER Jr, Ingram RH Jr, Jaeger JJ. Enhancement of exercise-induced asthma by cold air. N Engl J M e d 1977;297:743-7. 3. Deal EC J, McFadden ER Jr, Ingrain RH Jr, Jaeger JJ. In-
A I R W A Y REACTIVITY-INDUCED ASTHMA IN SINGERS
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Journal of Voice, Vol. 5, No. 4, 1991