Paradoxical Vocal Fold Motion Disorder in the Elite Athlete: Experience at a Large Division I University

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1 The Laryngoscope VC 2013 The American Laryngological, Rhinological and Otological Society, Inc. Paradoxical Vocal Fold Motion Disorder in the Elite Athlete: Experience at a Large Division I University Anna M. Marcinow, MD; Jennifer Thompson, MA, CCC-SLP; Tendy Chiang, MD; L. Arick Forrest, MD, MBA; Brad W. desilva, MD Objectives/Hypothesis: To review our experience at a large division I university with the diagnosis and management of paradoxical vocal fold motion disorder (PVFMD) in elite athletes. Study Design: A single institution retrospective review and cohort analysis. Methods: All elite athletes (division I collegiate athletes, triathletes, and marathon runners) with a diagnosis of PVFMD were identified. All patients underwent flexible fiberoptic laryngoscopy (FFL) to confirm the diagnosis of PVFMD. The type of PVFMD therapy was identified and efficacy of treatment was graded based on symptom resolution. Results: Forty-six consecutive athletes with PVFMD were identified. A total of 30/46 (65%) were division 1 collegiate athletes and 16/46 (35%) were triathletes or marathon runners. In comparison to a nonathlete PVFMD cohort, athletes were less likely to present with a history of reflux (P < 0.01), psychiatric diagnosis (P < 0.01), dysphonia (P < 0.01), cough (P ), or dysphagia (P < 0.01). The use of postexertion FFL provided additional diagnostic information in 11 (24%) patients. Laryngeal control therapy (LCT) was recommended for 45/46. A total of 36/45 attended at least one LCT session and 25 (69%) reported improvement of symptoms. Additionally, biofeedback, practice-observed therapy, and thyroarytenoid muscle botulinum toxin injection were required in three, two, and two patients, respectively. Conclusion: The addition of postexertion FFL improves the sensitivity to detect PVFMD in athletes. PVFMD in athletes responds well to LCT. However, biofeedback, practice-observed therapy, and botulinum toxin injection may be required for those patients with an inadequate response to therapy. Key Words: Paradoxical vocal fold dysfunction, athlete, dyspnea, laryngeal control therapy. Level of Evidence: 4. Laryngoscope, 124: , 2014 INTRODUCTION Paradoxical vocal fold motion disorder (PVFMD) is a dysfunction of the larynx defined as inappropriate closure of the vocal folds with respiration. 1 This subsequently results in partial, sometimes severe, obstruction of airflow and leads to attacks of shortness of breath, coughing and choking. Since the symptoms of PVFMD masquerade as other etiologies of shortness of breath, the diagnosis of PVFMD is commonly delayed 5 to 10 years. 2 Failure to recognize PVFMD and appropriately manage it may result in unnecessary treatments, including the use of inhaled beta2-adrenergic agonists and corticosteroids, 3 hospitalization, and even invasive mechanical ventilation. 4 From the Department of Otolaryngology Head and Neck Surgery (A.M.M., L.A.F., B.W.DS.); and the Department of Speech and Language Pathology J.T., Wexner Medical Center at The Ohio State University, Columbus, Ohio, U.S.A; and the Department of Otolaryngology (T.C.), University of Colorado School of Medicine, Aurora, Colorado, U.S.A. Editor s Note: This Manuscript was accepted for publication October 23, Presented at Triological Society annual meeting at the Combined Otolarygology Spring Meetings, Orlando, Florida, U.S.A., April 12 13, The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Brad W. desilva, MD, Department of Otolaryngology Head and Neck Surgery, The Ohio State University College of Medicine, 4019 W Dublin-Granville Rd, Dublin, OH Brad.DeSilva@osumc.edu DOI: /lary Rice et al. 5 previously speculated that PVFMD prevalence is as high as 3% among intercollegiate athletes. Rundell and Spiering 6 supported this finding in a study of 370 elite athletes with inspiratory stridor for which the incidence of PVFMD was 5%. The typical athlete with PVFMD has been described as a young female 1 with over-achieving personality traits and perceived psychosocial stressors. 7 Diagnosis of PVFMD requires direct visualization of the vocal folds while the patient is symptomatic and identifying inappropriate closure with respiration. 8 However, it can be especially challenging to simulate the physical and/or psychologic stresses of competition or practice in an artificial setting. 9 As such, Heinle et al. 10 suggest exercise laryngoscopy as a diagnostic method for PVFMD in athletes. With regard to treatment, reassurance to the patient that the condition is not life-threatening is the first intervention suggested Benzodiazepines have also been indicated for relief of symptoms 12,13 ; however, these medications can interfere with the performance status of an elite athlete. Heliox, a combination gas of helium and oxygen, has been suggested, but it is not practical outside the hospital setting. 14 Biofeedback, speech therapy, hypnosis, psychological therapy, and botulinum toxin have all been used with some variable success to treat chronic PVFMD. 11,13 17 The purpose of this retrospective review is to describe 1) the characteristics of PVFMD in the elite 1425

2 athlete, 2) our experience with the diagnosis of PVFMD in the elite athlete, and 3) the various interventions and their effectiveness at controlling symptoms of PVFMD during exercise. MATERIALS AND METHODS Study Design This was a retrospective chart review of elite athletes with newly diagnosed PVFMD that were evaluated at the Department of Otolaryngology Voice and Swallowing Clinic at the Ohio State University Wexner Medical Center. Approval was obtained from the institutional review board for this study. Inclusion Criteria All adult patients diagnosed with PVFMD between January 1, 2007, and December 31, 2011, were evaluated for inclusion in the study. Patients were classified as elite athletes if they reported an active history of collegiate level sport participation or marathon or triathlon training. Patients with incomplete medical records or failure to tolerate flexible fiberoptic laryngoscopy (FFL) were excluded from the study. The criteria for diagnosing PVFMD on FFL were as follows: 1. Observing respiration in the absence of gagging or coughing 2. Inappropriate adduction of the vocal folds during respiration, with at least two episodes per 10 respiratory cycles 3. Evidence of normal abduction at some point during the exam 4. Absence of other causes of airway obstruction Medical and Social History Clinical charts were reviewed for each patient to document history of 1) allergy, asthma, or inhaler/nebulizer use; 2) gastroesophageal reflux disease (GERD) and its treatment; 3) psychologic/psychiatric diagnoses and their treatment; 4) and respiratory symptoms during or after exertion. Patients were determined to have asthma if they had a history of positive results on pulmonary function testing or equivocal results with continued symptoms and inhaler use. They were determined to have GERD if they had a history of positive upper endoscopy or ph probe testing or if they self-reported the condition and used antacids. They were determined to have a psychiatric history if it was specifically listed as a diagnosis or if they reported being on medication with psychotropic effects, including antidepressants and anxiolytics. Physical Exam All of the subjects were evaluated by one of three experienced speech language pathologists (SLPs), with the diagnoses of PVFMD confirmed by a board certified otolaryngologist. The PVFMD evaluation protocol developed at our institution is listed in Table I and was used in the evaluation of all patients. 18 FFL was performed on all patients. When postexertional FFL was required, an exercise challenge was performed through the use of a stationary recumbent bike, sprinting on treadmill, or stair climbing until the patient became symptomatic and was immediately followed by FFL. Treatment Initial intervention consisted of laryngeal control therapy (LCT) performed by one of three experienced SLPs. The primary focus of LCT is neuromuscular reeducation of the vocal TABLE I. Evaluation Protocol for Patients With Suspected PVFMD. The SLP collects a case history including triggers for dyspnea. The patient is informed of the procedure and signs an informed consent form. The patient will be offered topical anesthetic, which will be administered by the physician. The flexible fiberoptic laryngoscope is passed via the nasal cavity to observe respiration at rest. The patient is directed to breathe in and out through the nose, in through the nose and out through the mouth, and in and out through the mouth. The patient holds breath for 5 seconds and then is directed to let it go. The patient is directed to count 1 to 10 on one breath. The patient is directed to count for as long as one breath can be held. If constriction is observed during normal respiration, the SLP will direct the patient in various therapeutic breathing techniques to discover what achieves full abduction. The exam will end at this point if the patient has shown constriction during normal respiration, and the patient will be enrolled in laryngeal control therapy. If constriction is not noted and exertion is a reported trigger, the patient will be directed to participate in activities for exertion until symptomatic (climbing stairs, riding a stationary bike, running on treadmill, jumping jacks). The scope will then be re-passed to observe glottal constriction during the presence of symptoms. Again, if constriction is observed, the patient will be directed in breathing therapy techniques to achieve abduction. In constriction is not observed at this point, the patient will be considered for a trial of laryngeal control therapy based on symptoms, history, and doctor recommendations. PVFMD 5 paradoxical vocal fold motion disorder; SLP 5 speech language pathologist. folds to assume an open, relaxed positioning during respiration. The SLP guides patients through identification of conditions that may contributing to PVFMD, treatment (when appropriate) of those contributing conditions, identification of dyspnea triggers, and instruction of laryngeal control breathing techniques (LCBTs) both at rest and with provocation (i.e., physical exertion, scent challenges, etc). LCBTs focus on noisy (turbulent) nasal inhalation, with lips closed tightly during inhalation, followed by noisy oral exhalation through puckered lips. These methods couple with diaphragmatic control to maximize breathing efficiency. Each patient practices this method using both continuous nasal inhalation (with closed lips at the time of inhalation), continuous oral exhalation (basic laryngeal control breathing), and multiple sniffs through the nose only (to augment the glottic inlet), followed by multiple pressurized puffs out through puckered lips (rescue laryngeal control breathing). When practiced and utilized regularly, these methods produce learned muscle memory establishing a relaxed vocal-fold position during respiration. Subsequent therapy sessions are designed to address each patient s triggers. Proactive use of LCBTs during provocation is highlighted in these sessions. Adjustments to the patients breathing during provocation are made as needed to achieve maximal relief from dyspnea. This may mean changing from basic to rescue laryngeal control breathing (especially with higher heart rates during physical provocation) or eliminating nasal inhalation and switching to sipping oral inhalation through puckered lips in order to avoid a smell trigger during desensitization. Typically, patients are seen two to four times and are discharged once they 1426

3 TABLE II. Characteristics of Athletes Diagnosed With PVFMD. Characteristic No. Patients (%) Total number of patients 46 Gender male 14 (%) female 32 (%) Age (median) 21 years, range years Athletic status collegiate athlete 30 (65%) marathon runner 13 (28%) triathlete 3 (7%) Associated symptoms shortness of breath 46 (100%) chest tightness 26 (57%) noisy breathing 21 (46%) throat tightness 19 (41%) cough 10 (22%) voice changes 7 (15%) Flattened inspiratory loop, yes (%) 19 (45%) Pretreatment inhaler use, yes (%) 37 (82%) Posttreatment inhaler use, yes (%) 8 (32%) GERD treatment, yes (%) 11 (24%) GERD, gastroesophageal reflux disease; PVFMD 5 paradoxical vocal fold motion disorder. demonstrate mastery of the breathing techniques and their symptoms are managed well. Patients were discharged from treatment once they had reached maximum benefit or symptom plateau. Patients who remained symptomatic were offered additional biofeedback or practice-observed sessions. During practice-observed sessions, the SLP attended the patient s workout facilities in order to observe the patient s use of breathing techniques in a more natural environment. An FFL exam was performed during all biofeedback sessions, allowing for direct observation of the effectiveness of each technique. In patients with improper nasal airflow preventing the teaching of proper breathing techniques, nasal steroid sprays and/or nasal airway surgery were offered as alternative treatments. Botulinum toxin injection into the thyroarytenoid muscle was considered for those patients with an inadequate response to LCT. Statistical Analysis Statistical analysis was performed on our study cohort using the InStat software (GraphPad Software, Inc, La Jolla, CA). Associations between clinical, pathological, and therapeutic variables and the risk of complications were assessed by v 2 test or t test when applicable. Differences were considered significant at P < RESULTS A total of 831 patients with PVFMD were identified through the medical records of the Ohio State University Voice and Swallowing Center. Of these, 54 (6%) patients were excluded due to incomplete medical records. From this cohort, 46 elite athletes with confirmed PVFMD (athlete cohort) were identified (Table II). The athlete cohort consisted of 14 male (30%) and 32 female (70%) patients. The median age at diagnosis was 21 years (range, years). Thirteen (28%) patients were marathon runners, three (7%) patients were triathletes, and 30 (65%) patients were active college-level athletes across a wide variety of sports (soccer, cross-country, softball, swimming, cheerleading, basketball, lacrosse, track and field, rowing, hockey). The most commonly noted symptoms, outside of shortness of breath, included cough (n 5 13), chest tightness (n 5 26), throat tightness (n 5 19), and noisy breathing (n 5 21). Only 30% of patients reported symptoms that were consistently reproducible with every exercise session. Comorbid conditions in the athlete cohort (Table III) included GERD in 13 (28%) patients, asthma in 18 (39%) patients, environmental allergies in 28 (46%) patients, psychiatric diagnosis in seven (15%) patients, and obstructive sleep apnea (OSA) in one (2%) patient. Forty-two (91%) patients underwent a thorough asthma evaluation through our institution s department of pulmonology, which included static pulmonary function testing (Table II). Of those, 19 (45%) patients were noted to have flattened inspiratory loops on spirometry. Eighty-two percent of patients were treated with asthma inhalers. Twenty (59%) patients reported no improvement, 13 (38%) patients reported partial improvement, and one (3%) patient reported a complete resolution of breathing symptoms with inhaler use. Following completion of PVFMD treatment, only 32% of patients reported continued inhaler use. Comparison of athlete cohort to an age- and gendermatched cohort of non-athletic PVFMD patients (nonathlete cohort) revealed that athletes were significantly TABLE III. Comparison of Past Medical History and Exam Findings in Athletes and Non-Athletes Diagnosed With PVFMD. Non- Athletes Athletes Yes No Yes No P Value Asthma GERD Psychiatric diagnosis Allergies COPD OSA Fibromyalgia Rheumatoid Arthritis Other pain disorder Laryngeal surgery Tobacco Alcohol Postcricoid edema Glottic lesion TVF Paresis COPD 5 chronic obstructive pulmonary disease; GERD 5 gastroesophageal reflux disease; OSA, obstructive sleep apnea; PVFMD 5 paradoxical vocal fold motion disorder; TVF 5 true vocal fold. 1427

4 TABLE IV. Results of Laryngeal Control Therapy Treatment in Elite Athletes Diagnosed With PVFMD. LCT Sessions Patients Improvement/Complete Resolution of Symptoms Discharged From Treatment 0 9 (20%) Outside facility 1 (2%) (24%) (27%) (27%) (26%) (83%) (50%) (22%) (90%) (80%) (7%) (100%) (100%) LCT 5 laryngeal control therapy. less likely to have associated GERD (P < 0.01) or psychiatric illness (P ) (Table III). These findings were supported by the patient s physical exam, where elite athletes were significantly less likely to have laryngeal edema noted on FFL (P ). All patients underwent FFL. Laryngeal lesions were noted on exam in five patients (11%) and included vocal fold ulceration and polypoid changes. A total of 6/46 patients were diagnosed by history alone, 28/46 were diagnosed with preexertion FFL, and 12/46 of the athletes were diagnosed by postexertion FFL. The remaining six patients (13%) did not have evidence of PVFMD on either testing method; however, further treatment was recommended based on strong patient history suggestive of PVFMD. The foundation of treatment consisted of LCT in all patients. The number of sessions attended and efficacy of treatment are outlined in Table IV. Nine (20%) patients were noncompliant and did not attend any LCT sessions. One (2%) patient completed therapy at an outside facility, and follow-up data was not available. A total of thirty-six (78%) patients completed at least one LCT session at our facility. Eleven (24%) patients completed one LCT session, 12 (26%) completed two sessions, 10 (22%) completed three sessions, and three (7%) patients completed four or more sessions. Of the patients who completed one session, three (27%) patients reported improvement or a complete resolution of symptoms. Ten (83%) patients who attended two therapy sessions reported improvement or a complete resolution of symptoms. Ninety percent of the patients who attended three LCT sessions reported improvement or resolution of symptoms. All of these patients who attended four or more LCT sessions reported improvement or a complete resolution of symptoms. The overall success rate for LCT, including patients who failed to follow up, was 43%. The average number of LCT sessions for improvement of respiratory symptoms was 2.5 and 2.6 in the athlete and non-athlete cohorts, respectively (P , CI 95%). Of the patients without sufficient response to LCT, three patients underwent biofeedback therapy, one patient underwent psychotherapy, six patients underwent the assessment of nasal airway, two patients underwent practice-observed therapy, and two patients underwent botulinum toxin injection into the thyroarytenoid muscles. In addition, athletic trainers accompanied two of the patients to their in-office LCT sessions. DISCUSSION The purpose of this study is to provide a comprehensive review of PVFMD in the elite athlete. We found that the majority of our patients presented to our clinic after failing to respond to various forms of pulmonary treatment. The sensitivity of PVFMD diagnosis was improved with the addition of postexertional FFL. PVFMD in athletes responds well to LCT. However, biofeedback, practice-observed therapy, and botulinum toxin injection may be required for those patients with an inadequate response to therapy. PVFMD and exercise-induced asthma (EIA) can present in strikingly similar manners and may even coexist. Newman et al. 4 documented the presence of asthma in as many as half of all patients diagnosed with PVFMD, and Morris et al. 13 reported evidence of coexistent asthma with PVFMD in 60% of their patients. In this study, we found that 18 (39%) of our athletes who presented to our clinic had previously received a diagnosis of EIA. and 39 (85%) had been started on inhalers. These findings were similar in our non-athlete cohort. Sixty-eight percent of the athletes were able to stop inhaler use following successful treatment of PVFMD. Patients who stopped inhaler use following treatment of PVFMD were more likely to have none or minimal response of symptoms to bronchodilators, or were started on an empiric trial of bronchodilators without objective evidence of EIA. EIA is defined as reversible airway obstruction that occurs during or after exertion. 19 Specific symptoms of EIA include chest tightness, wheezing, coughing, and shortness of breath, which result from acute bronchoconstriction. EIA symptoms typically peak 5 to 10 minutes after exercise begins and often spontaneously resolve within 30 to 60 minutes with continuous exercise. Coughing may persist for several hours after the cessation of activity, and the symptoms are typically reproducible under similar conditions. The symptoms most commonly reported in our study by patients diagnosed with PVFMD included shortness of breath, chest tightness, noisy breathing, throat tightness, cough, and voice changes, which are very similar to those reported in EIA. Koester at al. 20 previously reported that symptoms of throat tightness, dysphonia, audible noise on inspirations, or choking should raise suspicion for PVFMD. We found that 41% and 15% of patients reported throat tightness and voice changes, respectively. Often the diagnosis of PVFMD is not suspected until after treatments for EIA have not been effective in controlling the symptoms. This lack of symptomatic relief from bronchodilators has previously also been suggested to be an important discriminator between EIA 1428

5 and PVFMD. 4,7 The diagnosis can also be suspected by an incomplete or truncated inspiratory loop of the flowvolume curve during a PVFMD attack. 21,22 We observed this finding in 19 (45%) patients. We suspect that if pulmonary function testing had been performed during exertion, the number of patients with flattened inspiratory loops would have been even higher. Overall, we did not find a significant difference between athletes diagnosed with PVFMD when compared to a cohort of age-matched PVFMD patients who were not athletes. Our cohort of athletes did have lower rates of GERD (P ) and postcricoid edema of FFL (P ). This relationship between GERD and PVFMD is not well understood. One possible explanation is that the elite athlete cohort had lower rates of obesity, making them less predisposed to GERD; however, this study did not specifically examine this variable. Direct visualization of the upper airway (FFL) remains the gold standard for making a definitive diagnosis of PVFMD. 23,24 The classic pattern is adduction of the anterior two-thirds of the vocal cords with a posterior diamond-shaped chink. This occurs during inspiration, but it can be present during the entire respiratory cycle. 25,26 However, the diagnosis of PVFMD is sometimes difficult because it may be intermittent, especially in the elite athlete where the episodes may only be provoked by extreme exertion. Multiple maneuvers, such as breath holding and counting on a full breath, have been previously used to precipitate the abnormal closure of the vocal folds during inspiration and thus help diagnose the condition. However, we found that these maneuvers do not have the same diagnostic sensitivity in the elite athlete; the addition of postexertion FFL increased the sensitivity for PVFMD diagnosis from 58% to 83%. It is critical that the FFL be performed immediately following exertion while the patient s heart rate remained elevated and the patient is are symptomatic. However, even with the addition of postexertion testing, we had six athletes who failed to become symptomatic during in-office exertion, which was likely secondary to their high level of conditioning. Nevertheless, given a history highly suggestive of PVFMD, these patients were enrolled in a trial of treatment, and 50% reported a improvement in symptoms. This underlines the importance that symptoms may be difficult to elicit in the elite athlete, and a trial of LCT may be helpful in deducing the diagnosis of PVFMD. Once PVFMD is diagnosed, recommended treatments for exercise-induced symptoms have included speech therapy focusing on respiratory control, psychotherapy, hypnosis, biofeedback, injection of botulinum toxin, and heliox. 7,27 31 The specific form of speech therapy used for the treatment of PVFMD is known as LCT. We found this form of treatment effective in improving and/or resolving symptoms of PVFMD in 67% of our elite athletes, with effectiveness increasing to 88% in those who attended two or more LCT sessions. The premise of LCT focuses on two forms of breathing exercises: 1) diaphragmatic breathing, which allows the athlete to decrease upper body tension by retraining the abdominal muscles to expand during inhalation, thereby decreasing the tension in the chest, shoulder, and neck regions; and 2) rescue breathing, which allows the athlete to control or prevent an impending PVFMD attack. The athlete is trained to inhale quickly through the nose, followed by slow and relaxed exhalation through pursed lips at the first sign of an impending PVFMD attack. 32 In addition, we found that having the athletic trainer attend therapy or perform therapy in the patient s practice setting was helpful in reproducing the patient s symptoms and provide maximum benefit from treatment for some patients. In those patients without sufficient response to LCT, a suboptimal nasal airway may prohibit maximal benefit from LCT. Given that rescue breathing relies on inhaling through the nose to cause reflexive vocal fold abduction, significant nasal obstruction may prohibit this maneuver. Therefore, we found that correction of nasal obstruction (medically or surgically) in six of our patients allowed them to obtain maximal benefit from LCT. Last, botulinum toxin injection into the thyroarytenoid muscles was used in two patients who failed to improve with LCT with subsequent improvement in symptoms. CONCLUSION PVFMD in the athlete is frequently misdiagnosed as EIA. Alternatively the disorder may coexist with EIA. FFL remains the gold standard for diagnosis of PVFMD in the athlete; however, the addition of postexertional testing does improve the sensitivity of diagnostic testing. LCT is a well-tolerated and an effective method of managing PVFMD symptoms in athletes. In patients who fail to respond to LCT, biofeedback, practice observed therapy, treatment of nasal obstruction, and botulinum toxin injection are effective adjuvant treatment options. ACKNOWLEDGEMENT The authors thank the physicians at the Ohio State University Department of Pulmonology for their referral and collaboration with many of the participants in this study. The authors would also like to thank our speech language pathologists (Michelle Toth, Kerrie Obert, and Jennifer Thompson), who are instrumental in the diagnosis and treatment of our patients. BIBLIOGRAPHY 1. Brugman SM, Simons SM. Vocal cord dysfunction: don t mistake it for asthma. Physician Sportsmed 1998;26: Patel NJ, Jorgensen C, Kuhn J, Merati AL. Concurrent laryngeal abnormalities in patients with paradoxical vocal fold dysfunction. Otolaryngol Head Neck Surg 2004;130: Sullivan MD, Heywood BM, Beukelman DR. A treatment for vocal cord dysfunction in female athletes: an outcome study. 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