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Figure.
Simulation of the Experimental Protocol
Simulation of the Experimental Protocol

A, Participant seated upright, holding a flow meter to avoid obstructing the flow marker. B, Participant coughing once into a face mask that is tightly applied to face after inspiration.

Table 1.  
Participant Description and Peak Airflow Measurements Before and After Vocal Fold Augmentation
Participant Description and Peak Airflow Measurements Before and After Vocal Fold Augmentation
Table 2.  
Peak Airflow Measurements Collected From 4 Patients Before and Immediately After Vocal Fold Augmentation and at Follow-up Visit
Peak Airflow Measurements Collected From 4 Patients Before and Immediately After Vocal Fold Augmentation and at Follow-up Visit
1.
Troche  MS, Brandimore  AE, Okun  MS, Davenport  PW, Hegland  KW.  Decreased cough sensitivity and aspiration in Parkinson disease.  Chest. 2014;146(5):1294-1299.PubMedGoogle ScholarCrossref
2.
von Leden  H, Isshiki  N.  An analysis of cough at the level of the larynx.  Arch Otolaryngol. 1965;81(6):616-625.PubMedGoogle ScholarCrossref
3.
McCool  FD, Leith  DE.  Pathophysiology of cough.  Clin Chest Med. 1987;8(2):189-195.PubMedGoogle Scholar
4.
Hillel  AD.  The study of laryngeal muscle activity in normal human subjects and in patients with laryngeal dystonia using multiple fine-wire electromyography.  Laryngoscope. 2001;111(4, pt 2)(suppl 97):1-47.PubMedGoogle ScholarCrossref
5.
Kulnik  ST, Birring  SS, Hodsoll  J, Moxham  J, Rafferty  GF, Kalra  L.  Higher cough flow is associated with lower risk of pneumonia in acute stroke.  Thorax. 2016;71(5):474-475.PubMedGoogle ScholarCrossref
6.
Kulnik  ST, Rafferty  GF, Birring  SS, Moxham  J, Kalra  L.  A pilot study of respiratory muscle training to improve cough effectiveness and reduce the incidence of pneumonia in acute stroke: study protocol for a randomized controlled trial.  Trials. 2014;15:123.PubMedGoogle ScholarCrossref
7.
Britton  D, Benditt  JO, Merati  AL,  et al.  Associations between laryngeal and cough dysfunction in motor neuron disease with bulbar involvement.  Dysphagia. 2014;29(6):637-646.PubMedGoogle ScholarCrossref
8.
Mustfa  N, Moxham  J.  Respiratory muscle assessment in motor neurone disease.  QJM. 2001;94(9):497-502.PubMedGoogle ScholarCrossref
9.
Boitano  LJ.  Management of airway clearance in neuromuscular disease.  Respir Care. 2006;51(8):913-922.PubMedGoogle Scholar
10.
Toussaint  M, Boitano  LJ, Gathot  V, Steens  M, Soudon  P.  Limits of effective cough-augmentation techniques in patients with neuromuscular disease.  Respir Care. 2009;54(3):359-366.PubMedGoogle Scholar
11.
Plowman  EK, Watts  SA, Tabor  L,  et al.  Impact of expiratory strength training in amyotrophic lateral sclerosis.  Muscle Nerve. 2016;54(1):48-53.PubMedGoogle ScholarCrossref
12.
Pitts  T, Bolser  D, Rosenbek  J, Troche  M, Okun  MS, Sapienza  C.  Impact of expiratory muscle strength training on voluntary cough and swallow function in Parkinson disease.  Chest. 2009;135(5):1301-1308.PubMedGoogle ScholarCrossref
13.
Iwanaga  Y, Maeyama  T, Umezaki  T, Shin  T.  Intracordal injection increases glottic closing force in recurrent laryngeal nerve paralysis.  Otolaryngol Head Neck Surg. 1992;107(3):451-456.PubMedGoogle ScholarCrossref
14.
Ruddy  BH, Pitts  TE, Lehman  J, Spector  B, Lewis  V, Sapienza  CM.  Improved voluntary cough immediately following office-based vocal fold medialization injections.  Laryngoscope. 2014;124(7):1645-1647.PubMedGoogle ScholarCrossref
15.
Miller  MR, Hankinson  J, Brusasco  V,  et al; ATS/ERS Task Force.  Standardisation of spirometry.  Eur Respir J. 2005;26(2):319-338.PubMedGoogle ScholarCrossref
16.
Domer  AS, Kuhn  MA, Belafsky  PC.  Neurophysiology and clinical implications of the laryngeal adductor reflex.  Curr Otorhinolaryngol Rep. 2013;1(3):178-182.PubMedGoogle ScholarCrossref
17.
Boezen  HM, Schouten  JP, Postma  DS, Rijcken  B.  Distribution of peak expiratory flow variability by age, gender and smoking habits in a random population sample aged 20-70 yrs.  Eur Respir J. 1994;7(10):1814-1820.PubMedGoogle ScholarCrossref
18.
Sancho  J, Servera  E, Díaz  J, Marín  J.  Comparison of peak cough flows measured by pneumotachograph and a portable peak flow meter.  Am J Phys Med Rehabil. 2004;83(8):608-612.PubMedGoogle ScholarCrossref
Original Investigation
November 2017

Changes in Peak Airflow Measurement During Maximal Cough After Vocal Fold Augmentation in Patients With Glottic Insufficiency

Author Affiliations
  • 1NYU Voice Center, Department of Otolaryngology–Head and Neck Surgery, New York University School of Medicine, New York
  • 2NYU Department of Population Health, New York University School of Medicine, New York
  • 3Department of Mathematical Sciences, New Jersey Institute of Technology, Newark
JAMA Otolaryngol Head Neck Surg. 2017;143(11):1141-1145. doi:10.1001/jamaoto.2017.0976
Key Points

Question  Does vocal fold augmentation improve peak airflow during maximal cough in patients with glottic insufficiency?

Findings  In this case series study of 14 participants with glottic insufficiency, 11 participants experienced increased cough strength after vocal fold augmentation, with increased peak airflow ranging from 10 to 150 L/min.

Meaning  Change in peak airflow during maximal cough after vocal fold augmentation may lead to improved peak airflow during volitional cough, which is germane given the relationship between cough strength and aspiration, particularly in progressive neurologic disease.

Abstract

Importance  Compromised cough effectiveness is correlated with dysphagia and aspiration. Glottic insufficiency likely yields decreased cough strength and effectiveness. Although vocal fold augmentation favorably affects voice and likely improves cough strength, few data exist to support this hypothesis.

Objective  To assess whether vocal fold augmentation improves peak airflow measurements during maximal-effort cough following augmentation.

Design, Setting, and Participants  This case series study was conducted in a tertiary, academic laryngology clinic. Participants included 14 consecutive individuals with glottic insufficiency due to vocal fold paralysis, which was diagnosed via videostrobolaryngoscopy as a component of routine clinical examination. All participants who chose to proceed with augmentation were considered for the study whether office-based or operative augmentation was planned. Postaugmentation data were collected only at the first follow-up visit, which was targeted for 14 days after augmentation but varied on the basis of participant availability. Data were collected from June 5, 2014, to October 1, 2015. Data analysis took place between October 2, 2015, and March 3, 2017.

Main Outcomes and Measures  Peak airflow during maximal volitional cough was quantified before and after vocal fold augmentation. Participants performed maximal coughs, and peak expiratory flow during the maximal cough was captured according to American Thoracic Society guidelines.

Results  Among the 14 participants (7 men and 7 women), the mean (SD) age was 62 (18) years. Three types of injectable material were used for vocal fold augmentation: carboxymethylcellulose in 5 patients, hyaluronic acid in 5, and calcium hydroxylapatite in 4. Following augmentation, cough strength increased in 11 participants and decreased cough strength was observed in 3. Peak airflow measurements during maximal cough varied from a decrease of 40 L/min to an increase of 150 L/min following augmentation. When preaugmentation and postaugmentation peak airflow measurements were compared, the median improvement was 50 L/min (95% CI, 10-75 L/min; P = .01). Immediate peak airflow measurements during cough collected within 30 minutes of augmentation varied when compared with measurements collected at follow-up (103-380 vs 160-390 L/min).

Conclusions and Relevance  Peak airflow during maximal cough may improve with vocal fold augmentation. Additional assessment and measurements are needed to further delineate which patients will benefit most regarding their cough from vocal fold augmentation.

Introduction

One important role of cough is as a reflexive mechanism to protect the airway from aspiration. In conditions such as Parkinson disease, weak cough and reduced expiratory airflow values are associated with penetration and aspiration of bolus material.1 As described by von Leden and Isshiki,2 who used high-speed imaging, cough consists of 3 phases: inspiratory, compressive, and expiratory.2 Glottic closure is paramount to the compressive phase. Intrathoracic muscle contraction forcibly directs airflow up the trachea against a closed glottis, producing increased subglottal and intrathoracic pressures, which serve to accelerate the airstream in the expiratory phase to expel aspirated material.3 Glottic opening and laryngeal configuration during cough is further facilitated by the simultaneous activation of laryngeal muscles, both abductor and adductor muscles, in the compressive phase of cough, with adductor muscle relaxation at the initiation of expulsion.4

A direct correlation between increased cough strength and decreased pneumonia risk has been described.5 This finding is critical given the significant morbidity and mortality associated with pneumonia, particularly in the elderly. The role of cough strength in the prevention of aspiration is fundamental to improved poststroke care to prevent aspiration pneumonia and resulting morbidity.6 Cough dysfunction is prevalent in patients with motor neuron diseases, secondary to both altered lung function because of respiratory muscle weakness and impaired vocal fold function compared with that in healthy individuals.7,8 Peak airflow during maximal cough is currently used as a biomarker for implementing assisted cough therapies in patients with neuromuscular diseases.9,10 Cough strength has also been targeted therapeutically in at-risk populations, such as patients with amyotrophic lateral sclerosis and Parkinson disease.11,12

Despite the known link between cough strength and aspiration as well as the important role of the larynx in cough production, limited data assess enhanced glottic closure via vocal fold augmentation for the prevention of aspiration. Glottic closure pressure has been described following augmentation in unilateral recurrent laryngeal nerve paralysis in a feline model, although aspiration was not assessed.13 A recent study reported increased voluntary cough airflow in 3 patients immediately following augmentation; measurements were made within 30 minutes of vocal fold augmentation.14 No data exist regarding cough airflow beyond these immediate postinjection measurements made in a small cohort of 3 participants. The aim of this study was to evaluate changes in peak airflow during maximal cough following both in-office and operative vocal fold augmentation on a larger scale.

Methods

Fourteen consecutive individuals with glottic insufficiency secondary to unilateral vocal fold paralysis were prospectively recruited for participation in this study, which was conducted in a tertiary, academic laryngology clinic. Participants underwent quantification of peak airflow during maximal cough before and after vocal fold augmentation. Initially, the protocol involved data collection both immediately after augmentation (within 30 minutes) and at the first scheduled follow-up visit 14 days after the procedure. After the initial 4 participants were enrolled, however, the protocol was modified to collect postaugmentation data only at the first follow-up visit. This follow-up visit was targeted for 14 days after augmentation but varied on the basis of a participant’s availability to return to the clinic. This study was approved by the institutional review board of the New York University School of Medicine. Patient informed consent was obtained from each participant. Data were collected from June 5, 2014, to October 1, 2015. Data analysis took place between October 2, 2015, and March 3, 2017.

Glottic insufficiency related to unilateral vocal fold paralysis was diagnosed via videostrobolaryngoscopy as a component of routine clinical examination. All participants who chose to proceed with augmentation were considered for the study whether they, or the surgical team, planned office-based or operative augmentation. In addition, no discrimination was made between the injectable augmentation material used. Carboxymethylcellulose (Prolaryn; Merz or Renu; Bausch & Lomb), hyaluronic acid (Restylane; Galderma Laboratories or Juvederm; Allergan), or calcium hydroxylapatite (Prolaryn Plus; Merz) were used according to the clinical scenario, discussions with the participant, and clinical judgment. Medical records of participants were reviewed to identify history of pulmonary disease that might confound cough strength measurements, including chronic obstructive pulmonary disease, asthma, emphysema, and other restrictive or reactive lung diseases.

Peak flow meters (Mini Wright Peak Flow Meters; Clement Clarke) with a scale from 60 to 850 L/min or 30 to 400 L/min were used to collect peak airflow during maximal cough. If the smaller flow meter was used and a patient exceeded the capacity of the meter, peak airflow was tested again with the larger meter; this scenario was not encountered. A face mask covering the nares and oral cavity was used for each participant. A nose clip was not used because the American Thoracic Society (ATS) spirometry standardization guidelines do not require a nose clip for peak airflow measurements.15 Measures of peak airflow during maximal voluntary cough were obtained after participants decided to proceed with vocal fold augmentation and after consent but prior to any intervention.

To ensure reproducible, standardized cough-strength measurements, participants were carefully instructed on the experimental protocol, and the procedure was simulated by the investigators (Figure). Participants were seated upright in a comfortable position without restraining clothing, with their hands empty, and in a quiet environment. Following 3 normal breaths, they were instructed to take a deep breath, press the mask securely against their face to create a seal, and cough once as hard as possible. The meter was inspected for peak airflow value and reset for another attempt. Participant hand position was monitored to ensure there was no obstruction of the flow meter during data collection. Each participant completed 3 trials of maximal voluntary cough, and all 3 measurements were recorded. According to the ATS spirometry standards for peak airflow measurements, the 2 highest recordings were evaluated. If these values were within 40 L/min, the larger value was used for analysis.15 If the results were not reproducible within the recommended range, the mean peak airflow value was used and annotated in the results.

Statistical Analysis

Descriptive analyses were performed as well as the Wilcoxon signed rank test to compare preaugmentation and postaugmentation measures. An exact rank test was completed for the data set if ties were present, with 95% CIs included. Two-sided P = .01 was used to indicate statistical significance. All statistical analyses were performed using R software and RStudio software, version 0.99.879 (R).

Results

Fourteen participants completed preaugmentation and postaugmentation peak airflow measurements during maximal cough; results and demographics are included in Table 1. Seven men and seven women were included in the study, and participant age ranged from 30 to 83 years, with a mean (SD) age of 62 (18) years.

During data collection, all peak airflow measurements acquired at follow-up met ATS standardized peak airflow measurement criteria. During preaugmentation data collection, however, only 9 of 14 participants (64%) had peak airflow measurements that met ATS standardized peak airflow measurements. Of the 4 participants who also had immediate postaugmentation peak airflow measurements during maximal cough, 3 (75%) had peak airflow measurements that met ATS standardized peak airflow criteria.

Five of the 14 participants (36%) had a history of pulmonary disease (history of asthma, partial lung resection, and pulmonary embolism; recent aspiration pneumonia in 2); all of these participants had improved postaugmentation peak airflow measurements during maximal cough. Although targeted for 14 days, the number of days between augmentation and follow-up cough-strength assessment varied for patients because of their availability, with a median (interquartile range [IQR]) of 19 (12-37) days. Of the 14 participants, 11 (78%) underwent vocal fold augmentation in the clinic. All participants had improved glottic closure on videostrobolaryngoscopy during their follow-up visit. Review of these videostrobolaryngoscopy recordings from the 14 patients did not reveal differences in adequacy of glottic closure.

Peak airflow during maximal cough varied among participants at baseline, with a median of 150 L/min (range, 83-360 L/min) in both men and women prior to augmentation. Peak airflow values during a maximal cough increased in 11 of 14 participants following augmentation, with a median improvement in peak airflow of 50 L/min (overall improvement 95% CI, 10-75 L/min; P = .01). Cough strength decreased in 3 participants (2 women and 1 man); the magnitudes of decrease were 10, 37, and 40 L/min. All 3 participants with decreased peak airflow underwent in-office injections; the operative augmentation cohort was small (n = 3). All 5 participants with lung disease had improvement in their peak airflow during maximal cough after augmentation, with a median (IQR) of 63.5 L/min (10-140 L/min).

Post hoc analyses of augmentation material (carboxymethylcellulose [n = 5], hyaluronic acid [n = 5], or calcium hydroxylapatite [n = 4]) were then performed. Each group had 1 participant with decreased peak airflow during maximal cough. Among participants who improved, those who were augmented with hyaluronic acid had the greatest improvement (median [IQR] of 70 [5-150] L/min) compared with those who had carboxymethylcellulose and calcium hydroxylapatite augmentations (median [IQR] of 25 [10-77] L/min). The small subgroup within each type of augmentation material limited further statistical assessment.

As shown in Table 2, immediate improvement in maximal cough was noted and then further increase was observed at follow-up in 3 of the initial 4 participants who underwent peak airflow measurements during a maximal cough within 30 minutes of augmentation. In 1 participant, an initial decrease (−20 L/min) in peak airflow during maximal cough was noted immediately after augmentation that was then slightly elevated from baseline at the follow-up visit (an increase of 50 L/min compared with baseline). Only 1 of the 4 participants had stable airflow measurements during cough between the immediate postinjection measurements and follow-up. Statistical analyses of these results were not feasible because of the small sample size.

Discussion

Peak airflow during maximal cough varied among participants with glottic insufficiency and unilateral vocal fold paralysis after vocal fold augmentation. In 11 of 14 participants (78%), airflow during maximal cough increased following augmentation, concurring with a previous small study of 3 patients.14 The current study quantified airflow during a maximal cough beyond the acute postprocedure interval and included participants undergoing augmentation with a variety of injectable materials. Because the laryngeal vestibule is anesthetized for in-office augmentation, normal cough pathway sensory mechanisms and peak airflow measurements during a maximal cough may be altered.16 In addition, patients are generally not alert and awake enough to participate in these measurements within 30 minutes of vocal fold augmentation under general anesthesia in the operating room. Therefore, quantification of cough strength in the acute setting may not be particularly meaningful. In our initial 4 participants who underwent peak airflow measurements during maximal cough within 30 minutes of augmentation and again at a subsequent follow-up visit, differences were observed between the immediate and follow-up values for peak airflow during a maximal cough.

Peak airflow during maximal cough was most consistent after augmentation; ATS standardized peak airflow spirometry criteria were met in all 14 participants. Conversely, only 9 of 14 participants (64%) met ATS peak airflow criteria prior to augmentation. In the 5 participants (36%) who did not meet ATS criteria, more than a 40-L/min difference was observed between the 2 highest peak airflow recordings during maximal cough. For these patients, the mean peak airflow during maximal cough was selected to best account for variability in peak airflow recordings.

The recorded values of peak airflow during maximal cough were lower than those values reported for peak airflow measurement in the general population. Boezen et al17 sampled 520 participants and found the mean peak airflow in healthy individuals was 510 to 524 L/min depending on time of day (morning or evening); the SDs, however, were quite large: 113 and 112 L/min. No standard values derived from large population samples for peak airflow during maximal cough exist in the literature for individuals with vocal fold paralysis. In the 3 participants examined by Ruddy et al,14 expiratory-phase peak airflows ranged between 2.0 and 3.1 L/s (120-186 L/min) before vocal fold augmentation and between 2.8 and 4.0 L/s (168-240 L/min) after augmentation, which are within the range of the present study. Studies evaluating the peak airflow required to ensure adequate airway clearance in patients with neuromuscular diseases found that peak airflow measurements greater than 160 to 180 L/min were required for effective airway clearance.9,10 In our study, 12 of 14 participants (86%) met this threshold after augmentation, up from only 6 of 14 participants (43%) prior to augmentation. This increased peak airflow during maximal cough to above established thresholds in 75% of patients who were initially below this threshold may be a clinically relevant finding.

Follow-up intervals varied in this study, ranging from 12 to 37 days. However, all measurements occurred before injectate resorption would be anticipated. Interestingly, cough strength decreased in 3 participants. None of these participants had respiratory or neurologic dysfunction to explain these findings. Clinically, these participants had improved voice and videostrobolaryngoscopy at follow-up confirmed improved or complete glottal closure. Additional post hoc medical record review failed to identify factors that may explain this decreased airflow.

Limitations

This study is not without further limitations. Quantification of respiratory muscle strength was not performed for correlation to cough strength values. Respiratory muscle analysis would be particularly helpful in gaining mechanistic insight regarding the decrease in cough strength observed. In addition, the goal of this study was to assess volitional cough, which may differ from reflexive or spontaneous cough. Methodologically, a face mask attached to a peak flow meter was used for data collection. Although this method has been shown to be accurate in recording peak airflow measurement during a maximal cough and meets ATS criteria for peak airflow measurement during spirometry, this system does not collect subtle cough sequence nuances captured via a pneumotachometer. However, a study comparing peak airflow measurements using an oronasal mask connected to a pneumotachograph and a portable peak flow meter found no significant differences in peak airflow recordings among 62 participants between the 2 devices.18 Despite these limitations, this study supports the hypothesis that vocal fold augmentation altered peak airflow measurements during cough—a marker suggesting improved cough strength.

Conclusions

Peak airflow during maximal cough changed after vocal fold augmentation and may lead to improved peak airflow during volitional cough after augmentation. Additional assessment of factors that affect cough strength is needed to optimize cough strength in individuals with glottal insufficiency and to decrease aspiration risk and allow adequate cough strength for maximal expulsion of tracheobronchial contents.

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Article Information

Corresponding Author: Ryan C. Branski, PhD, NYU Voice Center, Department of Otolaryngology–Head and Neck Surgery, New York University School of Medicine, 345 E 37th St, Suite 306, New York, NY 10016 (ryan.branski@nyumc.org).

Accepted for Publication: May 10, 2017.

Published Online: July 13, 2017. doi:10.1001/jamaoto.2017.0976

Author Contributions: Drs Dion and Branski had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Dion, Persky, Branski, Amin.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Dion, Achlatis, Persky, Branski, Amin.

Critical revision of the manuscript for important intellectual content: Dion, Teng, Fang, Persky, Branski, Amin.

Statistical analysis: Dion, Achlatis, Fang.

Obtained funding: Persky.

Administrative, technical, or material support: Dion, Achlatis, Teng, Persky, Branski, Amin.

Study supervision: Branski, Amin.

Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest and none were reported.

Meeting Presentation: The results of this study were presented as a poster at the American Broncho-Esophagological Association Meeting at the Combined Otolaryngology Spring Meetings; May 19, 2016; Chicago, Illinois.

Additional Contributions: We thank the individual pictured in the Figure for granting permission to publish his image.

References
1.
Troche  MS, Brandimore  AE, Okun  MS, Davenport  PW, Hegland  KW.  Decreased cough sensitivity and aspiration in Parkinson disease.  Chest. 2014;146(5):1294-1299.PubMedGoogle ScholarCrossref
2.
von Leden  H, Isshiki  N.  An analysis of cough at the level of the larynx.  Arch Otolaryngol. 1965;81(6):616-625.PubMedGoogle ScholarCrossref
3.
McCool  FD, Leith  DE.  Pathophysiology of cough.  Clin Chest Med. 1987;8(2):189-195.PubMedGoogle Scholar
4.
Hillel  AD.  The study of laryngeal muscle activity in normal human subjects and in patients with laryngeal dystonia using multiple fine-wire electromyography.  Laryngoscope. 2001;111(4, pt 2)(suppl 97):1-47.PubMedGoogle ScholarCrossref
5.
Kulnik  ST, Birring  SS, Hodsoll  J, Moxham  J, Rafferty  GF, Kalra  L.  Higher cough flow is associated with lower risk of pneumonia in acute stroke.  Thorax. 2016;71(5):474-475.PubMedGoogle ScholarCrossref
6.
Kulnik  ST, Rafferty  GF, Birring  SS, Moxham  J, Kalra  L.  A pilot study of respiratory muscle training to improve cough effectiveness and reduce the incidence of pneumonia in acute stroke: study protocol for a randomized controlled trial.  Trials. 2014;15:123.PubMedGoogle ScholarCrossref
7.
Britton  D, Benditt  JO, Merati  AL,  et al.  Associations between laryngeal and cough dysfunction in motor neuron disease with bulbar involvement.  Dysphagia. 2014;29(6):637-646.PubMedGoogle ScholarCrossref
8.
Mustfa  N, Moxham  J.  Respiratory muscle assessment in motor neurone disease.  QJM. 2001;94(9):497-502.PubMedGoogle ScholarCrossref
9.
Boitano  LJ.  Management of airway clearance in neuromuscular disease.  Respir Care. 2006;51(8):913-922.PubMedGoogle Scholar
10.
Toussaint  M, Boitano  LJ, Gathot  V, Steens  M, Soudon  P.  Limits of effective cough-augmentation techniques in patients with neuromuscular disease.  Respir Care. 2009;54(3):359-366.PubMedGoogle Scholar
11.
Plowman  EK, Watts  SA, Tabor  L,  et al.  Impact of expiratory strength training in amyotrophic lateral sclerosis.  Muscle Nerve. 2016;54(1):48-53.PubMedGoogle ScholarCrossref
12.
Pitts  T, Bolser  D, Rosenbek  J, Troche  M, Okun  MS, Sapienza  C.  Impact of expiratory muscle strength training on voluntary cough and swallow function in Parkinson disease.  Chest. 2009;135(5):1301-1308.PubMedGoogle ScholarCrossref
13.
Iwanaga  Y, Maeyama  T, Umezaki  T, Shin  T.  Intracordal injection increases glottic closing force in recurrent laryngeal nerve paralysis.  Otolaryngol Head Neck Surg. 1992;107(3):451-456.PubMedGoogle ScholarCrossref
14.
Ruddy  BH, Pitts  TE, Lehman  J, Spector  B, Lewis  V, Sapienza  CM.  Improved voluntary cough immediately following office-based vocal fold medialization injections.  Laryngoscope. 2014;124(7):1645-1647.PubMedGoogle ScholarCrossref
15.
Miller  MR, Hankinson  J, Brusasco  V,  et al; ATS/ERS Task Force.  Standardisation of spirometry.  Eur Respir J. 2005;26(2):319-338.PubMedGoogle ScholarCrossref
16.
Domer  AS, Kuhn  MA, Belafsky  PC.  Neurophysiology and clinical implications of the laryngeal adductor reflex.  Curr Otorhinolaryngol Rep. 2013;1(3):178-182.PubMedGoogle ScholarCrossref
17.
Boezen  HM, Schouten  JP, Postma  DS, Rijcken  B.  Distribution of peak expiratory flow variability by age, gender and smoking habits in a random population sample aged 20-70 yrs.  Eur Respir J. 1994;7(10):1814-1820.PubMedGoogle ScholarCrossref
18.
Sancho  J, Servera  E, Díaz  J, Marín  J.  Comparison of peak cough flows measured by pneumotachograph and a portable peak flow meter.  Am J Phys Med Rehabil. 2004;83(8):608-612.PubMedGoogle ScholarCrossref
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