MILITARY MEDICINE, 178, 11:1208,2013
Vocal Cord Dysfunction Related to Combat Deployment COL Michael J. Morris, MC USA (Ret.)*; CPTRyan T. Cleszewski, MC USAf; MAJ James B. Stemer, MC USAf; Patrick F. Allan, MD§ ABSTRACT Objectives: Several etiologies for vocal cord dysfunction (VCD), a syndrome of dyspnea, noisy breathing, and inspiratory vocal cord closure are suggested; there is no consensus on the predisposition to its development. One previously identified psychiatric etiology is combat stress. Methods: A retrospective review of military personnel evaluated at Landstuhl Regional Medical Center with a new VCD diagnosis post-deployment was conducted. Medical records were reviewed for existing pulmonary, sinus, esophageal, or psychiatric disorders and determined their VCD evaluation. Results: Forty-eight patients were identified with VCD symptoms after combat deployment. For tnilitary personnel with VCD, symptoms were associated with several etiologies. Fifty-two percent reported symptoms were related to high stress/anxiety, whereas 39% reported symptoms during exercise; 16% had onset with acute respiratory illness and 7% were trauma related. The combination of a truncated inspiratory flow volume loop and negative methacholine challenge had a 72% positive predictive value. Conclusions: Common etiologies with VCD onset during deployment are anxiety/stress, exercise, or combination of factors. Spirometry with abnormal flow volume loop plus negative methacholine challenge testing offers a reasonable predictive value for diagnosing VCD. For deployed military with these findings, laryngoscopy for upper airway disorders should be conducted.
INTRODUCTION Vocal cord dysfunction (VCD) is a well-described syndrome defined by dyspnea, noisy breathing, and the presence of paradoxical vocal cord closure, primarily during inspiration, in the majority of patients.' Although several etiologies for VCD have been suggested based on typical presenting symptoms, there has been no established consensus on predisposing factors for development of symptomatic VCD. In the majority of cases, it is generally because of local glottic irritants (gastroesophageal reflux disease [GERD], postnasal drip, or various chemical exposures), exercise, or a wide assortment of psychiatric etiologies. It is frequently misdiagnosed as asthma in the clinical setting and is a commonly diagnosed condition in military personnel. A study of exertional dyspnea in military personnel demonstrated that 12% of patients evaluated had evidence of VCD most of which was exerciserelated.^ Emotional stress is frequently mentioned as a common precipitant of psychogenic VCD and may play an additional role in the mechanism for exercise-induced symptoms. Several studies highlight the importance of emotional Stressors as a primary trigger in psychogenic VCD. Gavin et al^ conducted a case-control study of pédiatrie VCD and asthma patients and found VCD patients tended to have significantly higher levels *Pulmonary/Critical Care Service, Department of Medicine, San Antonio Military Medical Center, 3551 Roger Brooke Drive, Fort Sam Houston, TX 78234. tHematology/Oncology Service, Department of Medicine, Walter Reed National Military Medical Center, 8901 Wisconsin Avenue, Bethesda, MD 20814. ^Allergy Service, Department of Medicine, William Beaumont Army Medical Center, 5005 North Piedras Street, El Paso, TX 79920. §Good Samaritan Hospital, 2222 Philadelphia Drive, Dayton, OH 45406. This article was presented at Army/Air Force Chapter American College of Physicians Regional Meeting November 2010. doi: 10.7205/MILMED-D-13-00155
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of anxiety and more anxiety-related diagnoses. Other Stressors such as competitive sports in young female athletes have been noted frequently as a trigger in exercise-induced VCD."*"^ In a military population, the majority of VCD patients have been young females between the ages of 20 and 40 often with a concomitant psychiatric diagnosis.^ The association between VCD and combat deployment has been previously described only as case reports. During the First Gulf War in 1991, two cases of deployed females with new onset respiratory symptoms that persisted post-deployment were described. In both patients, spirometry was normal between episodes and bronchoprovocation testing was negative as part of the evaluation for VCD.^ The objective of the study was to review VCD cases diagnosed at the level III evacuation center for U.S. military personnel from Operations Iraqi Freedom/Enduring Freedom (OIF/OEF) to provide an analysis of the causative factors and results of pulmonaiy evaluation of VCD for these deployed military personnel.
METHODS This study was conducted as a retrospective review of Department of Defense (DoD) medical records after obtaining written approval from the Brooke Army Medical Center Institutional Review Board. An investigator assigned to Landstuhl Regional Medical Center (LRMC) in southwest Germany during the review period (January 2005 to June 2009) identified from inpatient and outpatient medical records those patients diagnosed with VCD at the time of laryngoscopy. LRMC serves as the primary evacuation hospital for all U.S. military personnel for OIF/OEF who require a higher level of care not available or adequate in theater. After identifying these patients, the DoD electronic medical record was reviewed to identify essential clinical data concerning the diagnostic evaluation of VCD.
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Vocal Cord Dysfunction Related to Combat Deployment
Basic demographic information collected included age and gender of patients in addition to length and general location of deployment. Clinical information included frequency and duration of presenting clinical symptoms (dyspnea, chest pain, wheezing, stridor, changes in voice) and inciting event for clinical symptoms whether related to illness, injury, or trauma while in theater. Details of specific environmental particulate matter exposures such as bum pits or airborne chemicals were also extracted if specifically documented in the electronic medical record. Additional medical history included prior history of pulmonary or cardiac disease, medication use for asthma, allergic rhinitis, or GERD. The clinical evaluation was reviewed to include chest radiograph findings, laryngoscopy, and results of bronchoprovocation testing. Pulmonary function testing (PFT) values included forced expiratory volume at 1 second (FEV|), forced vital capacity (FVC), midexpiratory to inspiratory flow ratio (FEF/FIF50), post-bronchodilator (BD) FEV,, and overall appearance of the flow volume loop (FVL), particularly the inspiratory flow volume curve. A single inspiratory flow volume curve on the spirometry performed at the initial LRMC evaluation was reviewed by 2 investigators to determine evidence of truncation or flattening. Statistical analysis was performed using commercially available software (SPSS, version 19.0). Normality was tested for PFT variables and a student's t test or Mann-Whitney U test was used as appropriate between the 2 groups (normal vs. tmncated FVL). Specific comparisons were made for the following variables, FVC (% predicted), FEV, (% predicted), and FEV|/FVC (actual). Posthoc analysis was performed if the primary analysis failed to reach significance. Sensitivity, specificity, and positive predictive values were calculated for findings of an abnormal FVL and negative methacholine challenge testing (MCT). RESULTS Forty-eight patients, all active duty military personnel, were identified during the review of inpatient and outpatient medical records for the time period. The patient cohort included 22 males (46%) and 26 females (54%) with a tnean age of 31.2 ± 8.5 years. Eighty-four percent of the patients were U.S. Army personnel and the remaining 16% were assigned to the U.S. Air Force. Length and location of deployment were inconsistently documented (50%) in the electronic medical record. In those patients for whom complete deployment data were available (n = 24), 83% were deployed to Iraq for a mean period of 11.0 ± 5.2 months. The most common presenting clinical symptom was dyspnea, which was reported in 100% of the patients. Additional symptoms included chest pain (50%), wheezing (42%), and stridor (10%). As part of the initial evaluation, chest radiographs were performed on all patients and were normal without evidence of pulmonary disease. Only 15 of the 48 patients (31%) reported a specific environmental exposure to include smoke from bum pits, vehicle exhaust, or geologic dust. Documented inciting events for
MILITARY MEDICINE, Vol. 178, November 2013
Anxiety
Exercise
Anxiety/Exercise
D ALL {N=48)
13 Male (N=22)
Illness
Trauma
• Female {N=26)
Bar graph demonstrating the reported inciting cause for voeal cord dysfunction (in terms of percentage)
FIGURE 1.
Inciting cause for VCD.
airway symptoms (Fig. 1 ) were divided into several categories, with the majority of patients reporting anxiety or stress as a causative factor (35%), exercise (24%), upper respiratory illness (16%), traumatic injury (8%), and a combination of both anxiety and exercise (16%). Exercise was a more common precipitant in males whereas anxiety/stress was more common in females. Associated medical illnesses (based on medication profile) included treatment for GERD in 46% of patients and rhinitis symptoms in 60% of patients. Review of psychiatric diagnoses noted a formal diagnosis in 30 patients (63%); 12 males (55%) and 18 females (69%). Distribution of specific psychiatric diagnoses (depression, adjustment disorder, anxiety disorders, and others) is shown in Figure 2. There was no gender predominance for any specific psychiatric diagnosis in this cohort. Before pulmonary specialty evaluation, a diagnosis of asthma was documented in 10 of 48 (21%) patients and 31 of
69%
70%-
63%
H
60%50%42%
1
-— 30%-20%-- —
1—1—^Hin
35%
^H 29%
S|—
Ii-
10%-
31%
0%-i Psych Dx
Depression • AII(N=48)
Anxiety DMale(N=22)
Adjustment
Other Diagnoses
• Femaie (N=26)
Bar graph demonstrating the distribution (by percentage) of underlying diagnosed psychiatric disorders in patients with vocal cord dysfunction.
FIGURE 2.
Underlying psychiatric diagnoses.
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Vocal Cord Dysfunction Related to Combat Deployment TABLE I.
FT Values
Spirometry
All {N = 45)
Male (N = 22)
Female {N = 23)
p Value
FEV, (actual) FEV, (% predicted) FVC (actual) FVC (% predicted) FEVi/FVC FEF/FIF50 Post-BD Post-BD FEV, (actual) % Change FEV,
3.51 ±0.79 93.4 ± 15.8 4.24 ± 1.02 95.5 ± 16.7 83.2 ±8.1 I.Ol ±0.38 N = 35 3.39 ± 0.70 -0.77 ± 12.1
3.82 ± 0.79 94.1 ± 19.3 4.68 ±1.05 94.8 ± 19.8 82.8 ±4.8 0.98 ± 0.36 A'= 16 3.76 ± 0.65 1.5 ± 13.5
3.36 ±0.38 93.5 ± 10.0 3.73 ± 0.64 96.5 ±11.4 84.8 ± 10.2 1.08 ±0.43 A'=19 3.02 ± 0.52 -3.0 ± 9.7
NA 0.97 NA 0.66 0.18 0.19 NA 0.71
Student's t test used to compare differences in spirometry by gender (except for actual FEV,, actual FVC, and actual post-BD FEV, values). FEV,, forced expiratory volume at 1 second; FVC, forced vital capacity; FEF/FEF50, midexpiratory to inspiratory flow; BD, bronchodilator.
48 (65%) were treated with asthma medications at the time of VCD diagnosis. An inhaled corticosteroid/long-acting ßagonist was prescribed in 35%, an inhaled short-acting ßagonist in 47%, and 17% were taking a leukotriene receptor antagonist. There was no associated cardiac disease identified in any of the patients in this cohort. Flexible laxyngoscopy was performed both at rest and with exercise and identified the presence of paradoxical inspiratory true vocal cord closure in all patients as per the on-site investigator who evaluated most of the cohort. Spirometry was documented in the electronic medical record in 45 of 48 patients (94%) and the results are shown in Table I. All spirometry values shown are within normal reference ranges. There were no statistical differences between groups based on gender. There were only two patients with evidence of restrictive or obstructive indices. A post-BD FEV| was performed in 35 patients with a mean decrease of 0.77 ± 12.1% from baseline values. Two patients demonstrated a significant BD response (greater than 12% increase in FEVj) by American Thoracic Society standards. Review of the inspiratory FVL identified either truncated or flattened curves in 22 of 46 patients (48%). No statistically significant differences in spirometry parameters (FEVi, FVC, FEVi/FVC, or FEF/FIF50) were identified when comparing patients with normal and abnormal FVL (Table II). MCT was performed in 47 patients. Interpretation of the MCT reported increased bronchial responsiveness (greater than 20% reduction in FEVi) in 8 patients (17%) and negative MCT in the remaining 39 patients (83%). No documentation was available to review changes in the FVL during the performance of the MCT.*^ A
TABLE II.
FEV, (% predicted) FVC (% predicted) FBV,/FVC FEF/FIF50
FT and Inspiratory FVL Appearance Normal FVL
Truncated FVL
p Value
94.1 ± 19.3 94.8 ± 19.8 82.8 ±4.8 0.98 ± 0.36
93.5 ± 10.0 96.5 ±11.4 84.8 ± 10.2 1.08 ±0.43
0.97 0.66 0.18 0.19
Comparison of PFT values based on FVL appearance using student's t test. FEV,, forced expiratory volume at 1 second; FVC, forced vital capacity; FEF/FEF50, midexpiratory to inspiratory flow; FVL, flow volume loop.
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combination of both a truncated inspiratory FVL and a negative MCT resulted in a 72% positive predictive value for VCD in this cohort. DISCUSSION A significant portion of the published data on VCD has been extracted from the study of military personnel, but there is limited data on the specific etiology of causative factors in this population.^'^ There is no previous literature on the etiology of VCD from a deployed military population. As the primary evacuation hospital for the U.S. Central Command that receives patients from the theater of operations in southwest Asia, this facility regularly evaluates numerous patients with unexplained dyspnea or possible asthma. Numerous studies have documented the increased incidence of respiratory symptoms in the deployed military population."''" There were several notable findings from this primarily descriptive study. Roughly half of the deployed military population with VCD was female, which is significantly higher than the proportion of deployed military personnel who are female (~10%). Although combat stress and anxiety are the most common etiologies for VCD (50% of patients), there clearly are those patients with symptoms related to exercise, acute respiratory illness, or traumatic injuries. A significant percentage of patients (63%) were diagnosed with a variety of acute/chronic psychiatric illnesses, and many of these patients had underlying rhinitis (60%) and GERD (46%), which can potentially contribute to upper airway irritation, a significant factor in VCD symptoms. Findings suggestive of underlying airway hyper-responsiveness were limited as seen with only two patients with obstruction on spirometry and only 17% with a reactive MCT. Most patients in this cohort had a combination of normal spirometry and negative MCT with nearly 50% demonstrating abnormalities (truncation or flattening) on the inspiratory FVL. This combination resulted in a 72% positive predictive value for diagnosing VCD for this cohort. Etiologies for VCD may be generally classified into three predominant etiologies; exercise-induced, irritant-induced, and associated with underlying psychological disorders.'^ These different etiologies all represent a combination of underlying
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Vocal Cord Dysfunction Related to Combat Deployment
laryngeal sensitivity and an excessive response by glottis closure during inspiration.'''•''* Considerable overlap can be found between etiologies as demonstrated in this study where the causative factors were not solely related to the increased stress of deployment to a combat environment. The initial case reports of VCD emphasized the dominant underlying psychological disorders in this syndrome. The initial terminology of "Munchausen's sttidor," and "emotional laryngeal wheezing" suggested a psychological disorder as the etiology for inspiratory vocal cord adduction.'^'* The syndrome was typically described in young females working in the medical profession with significant emotional stress or psychiatric disease. A variety of functional disorders to include depression, sexual abuse, factitious disorder (intentional feigning of illness), and conversion disorder (symptoms with no definable cause) have all been recognized to be associated with VCD.' Christopher et al initially evaluated patients in 1983 and emphasized that these patients were unaware of their upper airway obstruction and were not purposely causing inspiratory vocal cord adduction. The patients in this cohort were predominantly found to have a conversion disorder.'^ An early descriptive VCD case series (« - 95) by Newman et al established the association of VCD with underlying psychiatric disorders. Nine of their patients had prior psychiatric hospitalizations and 73% were given a psychiatric diagnosis.'^ Even in the adolescent population, VCD patients compared to asthma controls showed higher incidence of significant psychiatric diagnoses to include major depression, separation anxiety, overanxious disorder, and dysthymia.^ The spectrum of psychiatric disorders associated with VCD is fairly broad. In a review of 48 VCD patients, the majority (52%) of patients were diagnosed with a conversion disorder, whereas 13% had a major depression, and 10% had a factitious disorder. The authors noted that underlying all these psychiatric diagnoses was the presence of significant emotional stress.'^ The authors commented that the increased female-to-male ratio, history of multiple hospitalizations, and numerous psychological symptoms found in conversion disorder correlated with the diagnosis of VCD. Other large studies found that 33 to 40% of VCD patients had underlying major depression.^'^° Exercise is also a commonly recognized precipitant of VCD and is reported as the underlying etiology in 18% of all patients. McFadden and Zawadski^ first reported seven elite athletes who presented with a "choking" sensation during exercise and had normal baseline spirometry and negative bronchoprovocation. A similar study evaluating adolescent athletes identified VCD on the basis of postexercise inspiratory FVL flattening.^' Exercise accounts for a significant percentage of VCD findings in military populations. In active duty military patients with exertional dyspnea, 12% of the patients had VCD, all of whom had symptoms precipitated primarily by exercise. Similarly, two other Army hospitals reported 52% of their VCD patients had exercise-induced symptoms.^ One unique characteristic of exercise-induced VCD is that patients tend to be highly competitive athletes
MILITARY MEDICINE, Vol. 178, November 2013
and the role of anxiety or stress also can be a predominant component of exercise-induced VCD.''"' Powell et al^ noted that 55% of 20 adolescent females with VCD had significant social stresses such as competitive sports. Treatment of exercise-induced symptoms can be highly effective with a combination of counseling and speech therapy.^^ Irritant-induced VCD is most related to intrinsic causes such as GERD or rhinitis/sinusitis or in certain individuals, extrinsic causes such as inhaled chemical irritants. The pathophysiology of irritant-associated VCD is hypothesized as accentuation of the glottic closure reflex caused by various extrinsic and intrinsic stimuli that trigger closure as a protective response.^'' Military personnel deployed to southwest Asia have been exposed to increased levels of airborne particulate matter since early in OIF/OEF.^^ Ambient particulate matter was collected from 15 locations throughout Iraq and Afghanistan over approximately a year; analysis demonstrated the three main air pollutant types to be geological dust, smoke from bum pits, and heavy metal condensates."^ These airborne materials found ubiquitously in the deployed environment may have caused increased upper airway irritation in susceptible individuals. The combination of either a viral upper respiratory illness or exposure while individuals were exercising in this environment may have been a contributing factor to the development of VCD symptoms. Similar to a previous study where 51% of military personnel surveyed had two or more risk factors for VCD such as GERD and allergic rhinitis, over 50% of our cohort were being treated for these disorders.^^ The more frequent appearance of a truncated inspiratory FVL at 50% in this study is higher than previous studies. A commonly reported finding in symptomatic VCD patients is presence of inspiratory FVL trtmcation or flattening consistent with variable extrathoracic obstruction. In these patients, the FVL may be helpful in suggesting the diagnosis of VCD, but a normal FVL, especially in asymptomatic individuals, does not exclude the diagnosis. The predictive value of the FVL to diagnose VCD has not been evaluated prospectively because of the intermittent nature of symptoms. The appearance of the inspiratory FVL in this study may have biased the initial selection of patients to undergo laryngoscopy at this center. Findings of an abnormal FVL for VCD in the literature are mixed. A review of spirometry with abnormal inspiratory FVL in patients who underwent a clinical evaluation noted that only 36% were diagnosed with VCD.^' In a study of VCD in military personnel with exertional dyspnea, only 20% of patients had an abnormal FVL at rest.^ Other retrospective studies have noted a 23% and 25% prevalence of inspiratory FVL abnormalities, respectively.'^'^** The ability of clinicians to predict VCD based on FVL appearance is limited with reported positive predictive values of 68% and 55% for two pulmonologists in a study of 226 patients undergoing laiyngoscopy.29 CONCLUSION Military personnel are a unique population deployed to many regions of the world that may be exposed to various levels of
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Vocal Cord Dysfunction Related to Combat Deployment
stress or anxiety in a combat environment. The current theaters of deployment in both Iraq and Afghanistan also may pose additional risk factors because of the higher levels of airborne particulate matter and potential hazards of geologic dusts. In the evaluation of dyspnea in deployed military personnel, it is necessary to keep VCD prominent on the differential diagnosis while performing an evaluation for other lung diseases such as asthma and interstitial lung diseases. Our cohort predominantly had normal spirometry and negative bronchoprovocation testing. In addition, a significant percentage of patients also had findings on the inspiratory FVL suggestive of a potential upper airway disorder. Both the high stress from combat environments and environmental exposures may contribute to the development of VCD. As shown in this study, the development of VCD in the deployed environment may be related to underlying psychiatric conditions, nonspecific upper airway irritation, and the significant stress of a combat environment.
11.
12. 13.
14. 15. 16. 17.
18. 19.
REFERENCES
20.
1. Morris MJ, Christopher KL: Diagnostic criteria for the classification of vocal cord dysfunction. Chest 2010; 138(5): 1213-23. 2. Morris MJ, Deal LE, Bean DR, Grbach VX, Morgan JA: Vocal cord dysfunction in patients with exertional dyspnea. Chest 1999; 116(6): 1676-82. 3. Gavin LA, Wamboldt M, Brugman S, Roesler TA, Wamboldt F: Psychological and family characteristics of adolescents with vocal cord dysfunction. J Asthma 1998; 35(5); 409-17. 4. McFadden ER, Zawadski DK; Vocal cord dysfunction masquerading as exercise-induced asthma a physiologic cause for "choking" during athletic activities. Am J Respir Crit Care Med 1996; 153(3); 942-7. 5. Powell DM, Karanfilov BI, Beechler KB, Treole K, Trudeau MD, Forrest LA; Paradoxical vocal cord dysfunction in juveniles. Arch Otolaryngol Head Neck Surg 2000; 126(1): 29-34. 6. Parker JM, Guerrero ML: Airway function in women; bronchial hyperresponsiveness, cough, and vocal cord dysfunction. Clin Chest Med 2004: 25(2): 321-30. 7. Craig T, Sitz K, Squire E, Smith L, Carpenter G: Vocal cord dysfunction during wartime. Mil Med 1992; 157(11); 614-6. 8. Perkins PJ, Morris MJ; Vocal cord dysfunction induced by methacholine challenge testing. Chest 2002; 122(6): 1988-93. 9. Perello MM, Gurevich J, Fitzpatrick T, Berg BW. Parker JM; Clinical characteristics of vocal cord dysfunction in two military tertiary care facilities. Am J Respir Crit Care Med 2003; 167; A788. 10. Smith B, Wong CA, Smith TC, Boyko EJ, Gacksetter GS, Ryan MAK; Newly reported respiratory symptoms and conditions among military
21.
1212
22.
23. 24.
25.
26.
27.
28. 29.
personnel deployed to Iraq and Afghanistan; a prospective populationbased study. Am J Epidemiol 2009; 170(11); 1433^42. Sanders JW, Putnam SD, Frankart C, et al; Impact of illness and noncombat injury during Operations Iraqi Freedom and Enduring Freedom (Afghanistan). Am J Trop Med Hyg 2005; 73; 713-9. Morris MJ, Allan PF, Perkins PJ; Vocal cord dysfunction; etiologies and treatment. Clin Pulm Med 2006; 13(2): 73-86. Ayres JG, Gabbott PL; Vocal cord dysfunction and laryngeal hyperresponsiveness: a function of altered autonomie balance? Thorax 2002; 57(4); 284-5. Morrison M, Rammage L, Emami AJ: The irritable larynx syndrome. J Voice 1999; 13(3); 447-55. Patterson R, Schatz M, Horton M; Munchausen's stridor: non-organic laryngeal obstruction. Clin Allergy 1974; 4(3): 307-10. Rodenstein DO, Francis C, Stanescu DC: Emotional laryngeal wheezing: a new syndrome. Am Rev Respir Dis 1983; 127(3); 354-6. Christopher KL, Wood RP, Eckert RC, Blager FB, Raney RA, Souhrada JF; Vocal cord dysfunction presenting as asthma. N Engl J Med 1983; 308(26); 1566-70. Newman KB, Mason UG III, Schmaling KB; Clinical features of vocal cord dysfunction. Am J Respir Crit Care Med 1995; 152(4 Pt 1); 1382-6. Lacy TJ, McManis SE; On vocal cord dysfunction. Mil Med 1993: 158(4); A4. Ramirez JR, Leon I, Rivera LM; Episodic laryngeal dyskinesia. Clinical and psychiatric characterization. Chest 1986; 90(5): 716-21. Landwehr LP, Wood RP II, Blager FB, Milgrom H: Vocal cord dysfunction mimicking exercise-induced bronchospasm in adolescents. Pediatrics 1996; 98(5); 971-4. Sullivan MD, Heywood BM, Beukelman DR; A treatment for vocal cord dysfunction in female athletes; an outcome study. Laryngoscope 2001; 111(10); 1751-5. Balkissoon R; Occupational upper airway disease. Clin Chest Med 2002; 23(4); 717-25. Weese CB, Abraham JH; Potential health implications associated with particulate matter exposure in deployed settings in southwest Asia. Inhal Toxicol2009; 21(4): 291-6. Engelbrecht JP, McDonald EV, Gillies JA, Jayanty RK, Casuccio G, Gertler AW: Characterizing mineral dusts and other aerosols from the Middle East—part 1: ambient sampling. Inhal Toxicol 2009; 21(4): 297-326. Gurevich-Uvena J, Parker JM, Fitzpatrick TM, et al: Medical comorbidities for paradoxical vocal fold motion (vocal cord dysfunction) in the military population. J Voice 2009; 24 (6): 728-31. Sterner JB, Morris MJ, Sill JM, Hayes JA: Inspiratory flow volume curve evaluation for detecting upper airway disease. Respir Care 2009; 54(4): 461-6. Perkner JJ, Fennelly KP, Balkissoon R, et al: Irritant-associated vocal cord dysfunction. J Occup Environ Med 1998; 40(2); 136-43. Watson MA, King CS, Holley AB, Greenburg DL, Mikita JA; Clinical and lung-function variables associated with vocal cord dysfunction. Respir Care 2009; 54(4); 467-73.
MILITARY MEDICINE, Vol. 178, Novetnber 2013
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Vocal Cord Dysfunction Related to Combat Deployment COL Michael J. Morris, MC USA (Ret.)*; CPTRyan T. Cleszewski, MC USAf; MAJ James B. Stemer, MC USAf; Patrick F. Allan, MD§ ABSTRACT Objectives: Several etiologies for vocal cord dysfunction (VCD), a syndrome of dyspnea, noisy breathing, and inspiratory vocal cord closure are suggested; there is no consensus on the predisposition to its development. One previously identified psychiatric etiology is combat stress. Methods: A retrospective review of military personnel evaluated at Landstuhl Regional Medical Center with a new VCD diagnosis post-deployment was conducted. Medical records were reviewed for existing pulmonary, sinus, esophageal, or psychiatric disorders and determined their VCD evaluation. Results: Forty-eight patients were identified with VCD symptoms after combat deployment. For tnilitary personnel with VCD, symptoms were associated with several etiologies. Fifty-two percent reported symptoms were related to high stress/anxiety, whereas 39% reported symptoms during exercise; 16% had onset with acute respiratory illness and 7% were trauma related. The combination of a truncated inspiratory flow volume loop and negative methacholine challenge had a 72% positive predictive value. Conclusions: Common etiologies with VCD onset during deployment are anxiety/stress, exercise, or combination of factors. Spirometry with abnormal flow volume loop plus negative methacholine challenge testing offers a reasonable predictive value for diagnosing VCD. For deployed military with these findings, laryngoscopy for upper airway disorders should be conducted.
INTRODUCTION Vocal cord dysfunction (VCD) is a well-described syndrome defined by dyspnea, noisy breathing, and the presence of paradoxical vocal cord closure, primarily during inspiration, in the majority of patients.' Although several etiologies for VCD have been suggested based on typical presenting symptoms, there has been no established consensus on predisposing factors for development of symptomatic VCD. In the majority of cases, it is generally because of local glottic irritants (gastroesophageal reflux disease [GERD], postnasal drip, or various chemical exposures), exercise, or a wide assortment of psychiatric etiologies. It is frequently misdiagnosed as asthma in the clinical setting and is a commonly diagnosed condition in military personnel. A study of exertional dyspnea in military personnel demonstrated that 12% of patients evaluated had evidence of VCD most of which was exerciserelated.^ Emotional stress is frequently mentioned as a common precipitant of psychogenic VCD and may play an additional role in the mechanism for exercise-induced symptoms. Several studies highlight the importance of emotional Stressors as a primary trigger in psychogenic VCD. Gavin et al^ conducted a case-control study of pédiatrie VCD and asthma patients and found VCD patients tended to have significantly higher levels *Pulmonary/Critical Care Service, Department of Medicine, San Antonio Military Medical Center, 3551 Roger Brooke Drive, Fort Sam Houston, TX 78234. tHematology/Oncology Service, Department of Medicine, Walter Reed National Military Medical Center, 8901 Wisconsin Avenue, Bethesda, MD 20814. ^Allergy Service, Department of Medicine, William Beaumont Army Medical Center, 5005 North Piedras Street, El Paso, TX 79920. §Good Samaritan Hospital, 2222 Philadelphia Drive, Dayton, OH 45406. This article was presented at Army/Air Force Chapter American College of Physicians Regional Meeting November 2010. doi: 10.7205/MILMED-D-13-00155
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of anxiety and more anxiety-related diagnoses. Other Stressors such as competitive sports in young female athletes have been noted frequently as a trigger in exercise-induced VCD."*"^ In a military population, the majority of VCD patients have been young females between the ages of 20 and 40 often with a concomitant psychiatric diagnosis.^ The association between VCD and combat deployment has been previously described only as case reports. During the First Gulf War in 1991, two cases of deployed females with new onset respiratory symptoms that persisted post-deployment were described. In both patients, spirometry was normal between episodes and bronchoprovocation testing was negative as part of the evaluation for VCD.^ The objective of the study was to review VCD cases diagnosed at the level III evacuation center for U.S. military personnel from Operations Iraqi Freedom/Enduring Freedom (OIF/OEF) to provide an analysis of the causative factors and results of pulmonaiy evaluation of VCD for these deployed military personnel.
METHODS This study was conducted as a retrospective review of Department of Defense (DoD) medical records after obtaining written approval from the Brooke Army Medical Center Institutional Review Board. An investigator assigned to Landstuhl Regional Medical Center (LRMC) in southwest Germany during the review period (January 2005 to June 2009) identified from inpatient and outpatient medical records those patients diagnosed with VCD at the time of laryngoscopy. LRMC serves as the primary evacuation hospital for all U.S. military personnel for OIF/OEF who require a higher level of care not available or adequate in theater. After identifying these patients, the DoD electronic medical record was reviewed to identify essential clinical data concerning the diagnostic evaluation of VCD.
MILITARY MEDICINE, Vol. 178, November 2013
Vocal Cord Dysfunction Related to Combat Deployment
Basic demographic information collected included age and gender of patients in addition to length and general location of deployment. Clinical information included frequency and duration of presenting clinical symptoms (dyspnea, chest pain, wheezing, stridor, changes in voice) and inciting event for clinical symptoms whether related to illness, injury, or trauma while in theater. Details of specific environmental particulate matter exposures such as bum pits or airborne chemicals were also extracted if specifically documented in the electronic medical record. Additional medical history included prior history of pulmonary or cardiac disease, medication use for asthma, allergic rhinitis, or GERD. The clinical evaluation was reviewed to include chest radiograph findings, laryngoscopy, and results of bronchoprovocation testing. Pulmonary function testing (PFT) values included forced expiratory volume at 1 second (FEV|), forced vital capacity (FVC), midexpiratory to inspiratory flow ratio (FEF/FIF50), post-bronchodilator (BD) FEV,, and overall appearance of the flow volume loop (FVL), particularly the inspiratory flow volume curve. A single inspiratory flow volume curve on the spirometry performed at the initial LRMC evaluation was reviewed by 2 investigators to determine evidence of truncation or flattening. Statistical analysis was performed using commercially available software (SPSS, version 19.0). Normality was tested for PFT variables and a student's t test or Mann-Whitney U test was used as appropriate between the 2 groups (normal vs. tmncated FVL). Specific comparisons were made for the following variables, FVC (% predicted), FEV, (% predicted), and FEV|/FVC (actual). Posthoc analysis was performed if the primary analysis failed to reach significance. Sensitivity, specificity, and positive predictive values were calculated for findings of an abnormal FVL and negative methacholine challenge testing (MCT). RESULTS Forty-eight patients, all active duty military personnel, were identified during the review of inpatient and outpatient medical records for the time period. The patient cohort included 22 males (46%) and 26 females (54%) with a tnean age of 31.2 ± 8.5 years. Eighty-four percent of the patients were U.S. Army personnel and the remaining 16% were assigned to the U.S. Air Force. Length and location of deployment were inconsistently documented (50%) in the electronic medical record. In those patients for whom complete deployment data were available (n = 24), 83% were deployed to Iraq for a mean period of 11.0 ± 5.2 months. The most common presenting clinical symptom was dyspnea, which was reported in 100% of the patients. Additional symptoms included chest pain (50%), wheezing (42%), and stridor (10%). As part of the initial evaluation, chest radiographs were performed on all patients and were normal without evidence of pulmonary disease. Only 15 of the 48 patients (31%) reported a specific environmental exposure to include smoke from bum pits, vehicle exhaust, or geologic dust. Documented inciting events for
MILITARY MEDICINE, Vol. 178, November 2013
Anxiety
Exercise
Anxiety/Exercise
D ALL {N=48)
13 Male (N=22)
Illness
Trauma
• Female {N=26)
Bar graph demonstrating the reported inciting cause for voeal cord dysfunction (in terms of percentage)
FIGURE 1.
Inciting cause for VCD.
airway symptoms (Fig. 1 ) were divided into several categories, with the majority of patients reporting anxiety or stress as a causative factor (35%), exercise (24%), upper respiratory illness (16%), traumatic injury (8%), and a combination of both anxiety and exercise (16%). Exercise was a more common precipitant in males whereas anxiety/stress was more common in females. Associated medical illnesses (based on medication profile) included treatment for GERD in 46% of patients and rhinitis symptoms in 60% of patients. Review of psychiatric diagnoses noted a formal diagnosis in 30 patients (63%); 12 males (55%) and 18 females (69%). Distribution of specific psychiatric diagnoses (depression, adjustment disorder, anxiety disorders, and others) is shown in Figure 2. There was no gender predominance for any specific psychiatric diagnosis in this cohort. Before pulmonary specialty evaluation, a diagnosis of asthma was documented in 10 of 48 (21%) patients and 31 of
69%
70%-
63%
H
60%50%42%
1
-— 30%-20%-- —
1—1—^Hin
35%
^H 29%
S|—
Ii-
10%-
31%
0%-i Psych Dx
Depression • AII(N=48)
Anxiety DMale(N=22)
Adjustment
Other Diagnoses
• Femaie (N=26)
Bar graph demonstrating the distribution (by percentage) of underlying diagnosed psychiatric disorders in patients with vocal cord dysfunction.
FIGURE 2.
Underlying psychiatric diagnoses.
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Vocal Cord Dysfunction Related to Combat Deployment TABLE I.
FT Values
Spirometry
All {N = 45)
Male (N = 22)
Female {N = 23)
p Value
FEV, (actual) FEV, (% predicted) FVC (actual) FVC (% predicted) FEVi/FVC FEF/FIF50 Post-BD Post-BD FEV, (actual) % Change FEV,
3.51 ±0.79 93.4 ± 15.8 4.24 ± 1.02 95.5 ± 16.7 83.2 ±8.1 I.Ol ±0.38 N = 35 3.39 ± 0.70 -0.77 ± 12.1
3.82 ± 0.79 94.1 ± 19.3 4.68 ±1.05 94.8 ± 19.8 82.8 ±4.8 0.98 ± 0.36 A'= 16 3.76 ± 0.65 1.5 ± 13.5
3.36 ±0.38 93.5 ± 10.0 3.73 ± 0.64 96.5 ±11.4 84.8 ± 10.2 1.08 ±0.43 A'=19 3.02 ± 0.52 -3.0 ± 9.7
NA 0.97 NA 0.66 0.18 0.19 NA 0.71
Student's t test used to compare differences in spirometry by gender (except for actual FEV,, actual FVC, and actual post-BD FEV, values). FEV,, forced expiratory volume at 1 second; FVC, forced vital capacity; FEF/FEF50, midexpiratory to inspiratory flow; BD, bronchodilator.
48 (65%) were treated with asthma medications at the time of VCD diagnosis. An inhaled corticosteroid/long-acting ßagonist was prescribed in 35%, an inhaled short-acting ßagonist in 47%, and 17% were taking a leukotriene receptor antagonist. There was no associated cardiac disease identified in any of the patients in this cohort. Flexible laxyngoscopy was performed both at rest and with exercise and identified the presence of paradoxical inspiratory true vocal cord closure in all patients as per the on-site investigator who evaluated most of the cohort. Spirometry was documented in the electronic medical record in 45 of 48 patients (94%) and the results are shown in Table I. All spirometry values shown are within normal reference ranges. There were no statistical differences between groups based on gender. There were only two patients with evidence of restrictive or obstructive indices. A post-BD FEV| was performed in 35 patients with a mean decrease of 0.77 ± 12.1% from baseline values. Two patients demonstrated a significant BD response (greater than 12% increase in FEVj) by American Thoracic Society standards. Review of the inspiratory FVL identified either truncated or flattened curves in 22 of 46 patients (48%). No statistically significant differences in spirometry parameters (FEVi, FVC, FEVi/FVC, or FEF/FIF50) were identified when comparing patients with normal and abnormal FVL (Table II). MCT was performed in 47 patients. Interpretation of the MCT reported increased bronchial responsiveness (greater than 20% reduction in FEVi) in 8 patients (17%) and negative MCT in the remaining 39 patients (83%). No documentation was available to review changes in the FVL during the performance of the MCT.*^ A
TABLE II.
FEV, (% predicted) FVC (% predicted) FBV,/FVC FEF/FIF50
FT and Inspiratory FVL Appearance Normal FVL
Truncated FVL
p Value
94.1 ± 19.3 94.8 ± 19.8 82.8 ±4.8 0.98 ± 0.36
93.5 ± 10.0 96.5 ±11.4 84.8 ± 10.2 1.08 ±0.43
0.97 0.66 0.18 0.19
Comparison of PFT values based on FVL appearance using student's t test. FEV,, forced expiratory volume at 1 second; FVC, forced vital capacity; FEF/FEF50, midexpiratory to inspiratory flow; FVL, flow volume loop.
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combination of both a truncated inspiratory FVL and a negative MCT resulted in a 72% positive predictive value for VCD in this cohort. DISCUSSION A significant portion of the published data on VCD has been extracted from the study of military personnel, but there is limited data on the specific etiology of causative factors in this population.^'^ There is no previous literature on the etiology of VCD from a deployed military population. As the primary evacuation hospital for the U.S. Central Command that receives patients from the theater of operations in southwest Asia, this facility regularly evaluates numerous patients with unexplained dyspnea or possible asthma. Numerous studies have documented the increased incidence of respiratory symptoms in the deployed military population."''" There were several notable findings from this primarily descriptive study. Roughly half of the deployed military population with VCD was female, which is significantly higher than the proportion of deployed military personnel who are female (~10%). Although combat stress and anxiety are the most common etiologies for VCD (50% of patients), there clearly are those patients with symptoms related to exercise, acute respiratory illness, or traumatic injuries. A significant percentage of patients (63%) were diagnosed with a variety of acute/chronic psychiatric illnesses, and many of these patients had underlying rhinitis (60%) and GERD (46%), which can potentially contribute to upper airway irritation, a significant factor in VCD symptoms. Findings suggestive of underlying airway hyper-responsiveness were limited as seen with only two patients with obstruction on spirometry and only 17% with a reactive MCT. Most patients in this cohort had a combination of normal spirometry and negative MCT with nearly 50% demonstrating abnormalities (truncation or flattening) on the inspiratory FVL. This combination resulted in a 72% positive predictive value for diagnosing VCD for this cohort. Etiologies for VCD may be generally classified into three predominant etiologies; exercise-induced, irritant-induced, and associated with underlying psychological disorders.'^ These different etiologies all represent a combination of underlying
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Vocal Cord Dysfunction Related to Combat Deployment
laryngeal sensitivity and an excessive response by glottis closure during inspiration.'''•''* Considerable overlap can be found between etiologies as demonstrated in this study where the causative factors were not solely related to the increased stress of deployment to a combat environment. The initial case reports of VCD emphasized the dominant underlying psychological disorders in this syndrome. The initial terminology of "Munchausen's sttidor," and "emotional laryngeal wheezing" suggested a psychological disorder as the etiology for inspiratory vocal cord adduction.'^'* The syndrome was typically described in young females working in the medical profession with significant emotional stress or psychiatric disease. A variety of functional disorders to include depression, sexual abuse, factitious disorder (intentional feigning of illness), and conversion disorder (symptoms with no definable cause) have all been recognized to be associated with VCD.' Christopher et al initially evaluated patients in 1983 and emphasized that these patients were unaware of their upper airway obstruction and were not purposely causing inspiratory vocal cord adduction. The patients in this cohort were predominantly found to have a conversion disorder.'^ An early descriptive VCD case series (« - 95) by Newman et al established the association of VCD with underlying psychiatric disorders. Nine of their patients had prior psychiatric hospitalizations and 73% were given a psychiatric diagnosis.'^ Even in the adolescent population, VCD patients compared to asthma controls showed higher incidence of significant psychiatric diagnoses to include major depression, separation anxiety, overanxious disorder, and dysthymia.^ The spectrum of psychiatric disorders associated with VCD is fairly broad. In a review of 48 VCD patients, the majority (52%) of patients were diagnosed with a conversion disorder, whereas 13% had a major depression, and 10% had a factitious disorder. The authors noted that underlying all these psychiatric diagnoses was the presence of significant emotional stress.'^ The authors commented that the increased female-to-male ratio, history of multiple hospitalizations, and numerous psychological symptoms found in conversion disorder correlated with the diagnosis of VCD. Other large studies found that 33 to 40% of VCD patients had underlying major depression.^'^° Exercise is also a commonly recognized precipitant of VCD and is reported as the underlying etiology in 18% of all patients. McFadden and Zawadski^ first reported seven elite athletes who presented with a "choking" sensation during exercise and had normal baseline spirometry and negative bronchoprovocation. A similar study evaluating adolescent athletes identified VCD on the basis of postexercise inspiratory FVL flattening.^' Exercise accounts for a significant percentage of VCD findings in military populations. In active duty military patients with exertional dyspnea, 12% of the patients had VCD, all of whom had symptoms precipitated primarily by exercise. Similarly, two other Army hospitals reported 52% of their VCD patients had exercise-induced symptoms.^ One unique characteristic of exercise-induced VCD is that patients tend to be highly competitive athletes
MILITARY MEDICINE, Vol. 178, November 2013
and the role of anxiety or stress also can be a predominant component of exercise-induced VCD.''"' Powell et al^ noted that 55% of 20 adolescent females with VCD had significant social stresses such as competitive sports. Treatment of exercise-induced symptoms can be highly effective with a combination of counseling and speech therapy.^^ Irritant-induced VCD is most related to intrinsic causes such as GERD or rhinitis/sinusitis or in certain individuals, extrinsic causes such as inhaled chemical irritants. The pathophysiology of irritant-associated VCD is hypothesized as accentuation of the glottic closure reflex caused by various extrinsic and intrinsic stimuli that trigger closure as a protective response.^'' Military personnel deployed to southwest Asia have been exposed to increased levels of airborne particulate matter since early in OIF/OEF.^^ Ambient particulate matter was collected from 15 locations throughout Iraq and Afghanistan over approximately a year; analysis demonstrated the three main air pollutant types to be geological dust, smoke from bum pits, and heavy metal condensates."^ These airborne materials found ubiquitously in the deployed environment may have caused increased upper airway irritation in susceptible individuals. The combination of either a viral upper respiratory illness or exposure while individuals were exercising in this environment may have been a contributing factor to the development of VCD symptoms. Similar to a previous study where 51% of military personnel surveyed had two or more risk factors for VCD such as GERD and allergic rhinitis, over 50% of our cohort were being treated for these disorders.^^ The more frequent appearance of a truncated inspiratory FVL at 50% in this study is higher than previous studies. A commonly reported finding in symptomatic VCD patients is presence of inspiratory FVL trtmcation or flattening consistent with variable extrathoracic obstruction. In these patients, the FVL may be helpful in suggesting the diagnosis of VCD, but a normal FVL, especially in asymptomatic individuals, does not exclude the diagnosis. The predictive value of the FVL to diagnose VCD has not been evaluated prospectively because of the intermittent nature of symptoms. The appearance of the inspiratory FVL in this study may have biased the initial selection of patients to undergo laryngoscopy at this center. Findings of an abnormal FVL for VCD in the literature are mixed. A review of spirometry with abnormal inspiratory FVL in patients who underwent a clinical evaluation noted that only 36% were diagnosed with VCD.^' In a study of VCD in military personnel with exertional dyspnea, only 20% of patients had an abnormal FVL at rest.^ Other retrospective studies have noted a 23% and 25% prevalence of inspiratory FVL abnormalities, respectively.'^'^** The ability of clinicians to predict VCD based on FVL appearance is limited with reported positive predictive values of 68% and 55% for two pulmonologists in a study of 226 patients undergoing laiyngoscopy.29 CONCLUSION Military personnel are a unique population deployed to many regions of the world that may be exposed to various levels of
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Vocal Cord Dysfunction Related to Combat Deployment
stress or anxiety in a combat environment. The current theaters of deployment in both Iraq and Afghanistan also may pose additional risk factors because of the higher levels of airborne particulate matter and potential hazards of geologic dusts. In the evaluation of dyspnea in deployed military personnel, it is necessary to keep VCD prominent on the differential diagnosis while performing an evaluation for other lung diseases such as asthma and interstitial lung diseases. Our cohort predominantly had normal spirometry and negative bronchoprovocation testing. In addition, a significant percentage of patients also had findings on the inspiratory FVL suggestive of a potential upper airway disorder. Both the high stress from combat environments and environmental exposures may contribute to the development of VCD. As shown in this study, the development of VCD in the deployed environment may be related to underlying psychiatric conditions, nonspecific upper airway irritation, and the significant stress of a combat environment.
11.
12. 13.
14. 15. 16. 17.
18. 19.
REFERENCES
20.
1. Morris MJ, Christopher KL: Diagnostic criteria for the classification of vocal cord dysfunction. Chest 2010; 138(5): 1213-23. 2. Morris MJ, Deal LE, Bean DR, Grbach VX, Morgan JA: Vocal cord dysfunction in patients with exertional dyspnea. Chest 1999; 116(6): 1676-82. 3. Gavin LA, Wamboldt M, Brugman S, Roesler TA, Wamboldt F: Psychological and family characteristics of adolescents with vocal cord dysfunction. J Asthma 1998; 35(5); 409-17. 4. McFadden ER, Zawadski DK; Vocal cord dysfunction masquerading as exercise-induced asthma a physiologic cause for "choking" during athletic activities. Am J Respir Crit Care Med 1996; 153(3); 942-7. 5. Powell DM, Karanfilov BI, Beechler KB, Treole K, Trudeau MD, Forrest LA; Paradoxical vocal cord dysfunction in juveniles. Arch Otolaryngol Head Neck Surg 2000; 126(1): 29-34. 6. Parker JM, Guerrero ML: Airway function in women; bronchial hyperresponsiveness, cough, and vocal cord dysfunction. Clin Chest Med 2004: 25(2): 321-30. 7. Craig T, Sitz K, Squire E, Smith L, Carpenter G: Vocal cord dysfunction during wartime. Mil Med 1992; 157(11); 614-6. 8. Perkins PJ, Morris MJ; Vocal cord dysfunction induced by methacholine challenge testing. Chest 2002; 122(6): 1988-93. 9. Perello MM, Gurevich J, Fitzpatrick T, Berg BW. Parker JM; Clinical characteristics of vocal cord dysfunction in two military tertiary care facilities. Am J Respir Crit Care Med 2003; 167; A788. 10. Smith B, Wong CA, Smith TC, Boyko EJ, Gacksetter GS, Ryan MAK; Newly reported respiratory symptoms and conditions among military
21.
1212
22.
23. 24.
25.
26.
27.
28. 29.
personnel deployed to Iraq and Afghanistan; a prospective populationbased study. Am J Epidemiol 2009; 170(11); 1433^42. Sanders JW, Putnam SD, Frankart C, et al; Impact of illness and noncombat injury during Operations Iraqi Freedom and Enduring Freedom (Afghanistan). Am J Trop Med Hyg 2005; 73; 713-9. Morris MJ, Allan PF, Perkins PJ; Vocal cord dysfunction; etiologies and treatment. Clin Pulm Med 2006; 13(2): 73-86. Ayres JG, Gabbott PL; Vocal cord dysfunction and laryngeal hyperresponsiveness: a function of altered autonomie balance? Thorax 2002; 57(4); 284-5. Morrison M, Rammage L, Emami AJ: The irritable larynx syndrome. J Voice 1999; 13(3); 447-55. Patterson R, Schatz M, Horton M; Munchausen's stridor: non-organic laryngeal obstruction. Clin Allergy 1974; 4(3): 307-10. Rodenstein DO, Francis C, Stanescu DC: Emotional laryngeal wheezing: a new syndrome. Am Rev Respir Dis 1983; 127(3); 354-6. Christopher KL, Wood RP, Eckert RC, Blager FB, Raney RA, Souhrada JF; Vocal cord dysfunction presenting as asthma. N Engl J Med 1983; 308(26); 1566-70. Newman KB, Mason UG III, Schmaling KB; Clinical features of vocal cord dysfunction. Am J Respir Crit Care Med 1995; 152(4 Pt 1); 1382-6. Lacy TJ, McManis SE; On vocal cord dysfunction. Mil Med 1993: 158(4); A4. Ramirez JR, Leon I, Rivera LM; Episodic laryngeal dyskinesia. Clinical and psychiatric characterization. Chest 1986; 90(5): 716-21. Landwehr LP, Wood RP II, Blager FB, Milgrom H: Vocal cord dysfunction mimicking exercise-induced bronchospasm in adolescents. Pediatrics 1996; 98(5); 971-4. Sullivan MD, Heywood BM, Beukelman DR; A treatment for vocal cord dysfunction in female athletes; an outcome study. Laryngoscope 2001; 111(10); 1751-5. Balkissoon R; Occupational upper airway disease. Clin Chest Med 2002; 23(4); 717-25. Weese CB, Abraham JH; Potential health implications associated with particulate matter exposure in deployed settings in southwest Asia. Inhal Toxicol2009; 21(4): 291-6. Engelbrecht JP, McDonald EV, Gillies JA, Jayanty RK, Casuccio G, Gertler AW: Characterizing mineral dusts and other aerosols from the Middle East—part 1: ambient sampling. Inhal Toxicol 2009; 21(4): 297-326. Gurevich-Uvena J, Parker JM, Fitzpatrick TM, et al: Medical comorbidities for paradoxical vocal fold motion (vocal cord dysfunction) in the military population. J Voice 2009; 24 (6): 728-31. Sterner JB, Morris MJ, Sill JM, Hayes JA: Inspiratory flow volume curve evaluation for detecting upper airway disease. Respir Care 2009; 54(4): 461-6. Perkner JJ, Fennelly KP, Balkissoon R, et al: Irritant-associated vocal cord dysfunction. J Occup Environ Med 1998; 40(2); 136-43. Watson MA, King CS, Holley AB, Greenburg DL, Mikita JA; Clinical and lung-function variables associated with vocal cord dysfunction. Respir Care 2009; 54(4); 467-73.
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