Chest ACCP Member Benefits
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Guest Access | Sign In via User Name/Password
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (21)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sancho, J.
Right arrow Articles by Marín, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sancho, J.
Right arrow Articles by Marín, J.
(Chest. 2004;125:1400-1405.)
© 2004 American College of Chest Physicians

Efficacy of Mechanical Insufflation-Exsufflation in Medically Stable Patients With Amyotrophic Lateral Sclerosis*

Jesús Sancho, MD; Emilio Servera, MD, FCCP; Juan Díaz, RN and Julio Marín, MD, FCCP

* From the Department of Respiratory Medicine, Hospital Clínico Universitario, Universitat de València, Valencia, Spain.

Correspondence to: Emilio Servera MD, FCCP, Avda Blasco Ibáñez 84, E 46021 Valencia, Spain; e-mail: emilio.servera{at}uv.es


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objective: To determine under what circumstances the use of mechanical insufflation-exsufflation (MI-E) can generate clinically effective expiratory flows for airway clearance (> 2.7 L/s) for clinically stable patients with amyotrophic lateral sclerosis (ALS).

Materials and method: Twenty-six consecutive patients with ALS were studied, 15 with severe bulbar dysfunction. Using a pneumotachograph and with the aid of an oronasal mask, we measured FVC, FEV1, peak cough flow (PCF), maximum insufflation capacity (MIC), PCF generated from a maximum insufflation MIC (PCFMIC), and PCF generated by MI-E (PCFMI-E). MI-E was delivered at ± 40 cm H2O. Maximum inspiratory pressure (PImax) and maximum expiratory pressure (PEmax) at the mouth were also measured.

Results: Although both groups had a similar time from ALS symptom onset to diagnosis, statistical differences (p < 0.05) were found between nonbulbar and bulbar patients in lung function and cough capacity parameters: FVC, 2.58 ± 1.24 L vs 1.62 ± 0.74 L; FEV1, 2.26 ± 1.18 L vs 1.54 ± 0.69 L; PImax, – 93.45 ± 47.47 cm H2O vs – 3.64 ± 25.07 cm H2O; PEmax, 140.45 ± 75.98 cm H2O vs 69.93 ± 32.14 cm H2O; MIC, 3.02 ± 1.22 L vs 1.97 ± 0.75 L; PCF, 5.91 ± 2.55 L/s vs 3.42 ± 1.44 L/s; PCFMIC, 6.68 ± 2.71 L/s vs 4.00 ± 1.48 L/s; and PCFMI-E, 4.34 ± 0.82 L/s vs 3.35 ± 0.77 L/s. Four patients with bulbar dysfunction and MIC > 1 L had PCFMI-E < 2.7 L/s. The receiver operating characteristic (ROC) curve analysis showed PCFMIC of <= 2.7 L/s predicting those patients with PCFMI-E < 2.7 L/s. The ROC curve analysis showed PCFMIC > 4 L/s predicting those patients with PCFMIC greater than PCFMI-E.

Conclusion: MI-E is able to generate clinically effective PCFMI-E (> 2.7 L/s) for stable patients with ALS, except for those with bulbar dysfunction who also have a MIC > 1 L and PCFMIC <2.7 L/s who probably have severe dynamic collapse of the upper airways during the exsufflation cycle. Clinically stable patients with mild respiratory dysfunction and PCFMIC > 4 L/s might not benefit from MI-E except during an acute respiratory illness.

Key Words: amyotrophic lateral sclerosis • cough capacity • lung function test • mechanical insufflation-exsufflation • neuromuscular disease • noninvasive respiratory aids • noninvasive ventilation • peak cough flow


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Amyotrophic lateral sclerosis (ALS) is a progressive motorneuron disease. Inspiratory, expiratory, and upper airway muscles become impaired.1 Respiratory complications, and especially airway secretion encumberment from ineffective coughing, are the principal causes of morbidity and mortality.2

Coughing is a key defense mechanism of the airways. The effectiveness of mucus clearance is largely dependent on the magnitude of peak cough flows (PCFs).3 Respiratory muscle weakness decreases PCF and, thereby, diminishes cough effectiveness. There are few data regarding a cutoff point for cough effectiveness. However, a PCF of < 2.7 L/s has been proposed as indicating an ineffective cough on the basis of flows below this level resulting in extubation failure.4 Baseline PCF values < 4.5 L/s have also been reported to be associated with a high risk for pulmonary complications during respiratory tract infections5 because during chest infections the pressure generated by expiratory muscles is reduced6 and, consequently, PCF decreases further. However these cutoff PCF values must be taken with caution and not as precise guidelines to predict cough failure, because they are not based on prospective trial results.

The use of inspiratory and expiratory aids has been reported to reduce the risk of pulmonary complications and prolong survival.7 Mechanical ventilation, noninvasive or via tracheostomy, is able to prevent or reverse ventilatory failure for patients with ALS or other neuromuscular diseases.8 More attention now needs to be paid to clearing airway secretions.

Assisted coughing techniques, both manual and mechanical, can increase PCF over unassisted levels and, thus, increase airway clearance capacity.9 Manually assisted coughing requires patient and caregiver cooperation and involves the use of an abdominal thrust following attainment of lung volumes approaching the maximum insufflation capacity (MIC). This is achieved by using a manual resuscitator or a portable volume ventilator to "stack" volumes of air into the lungs, holding them with a closed glottis.10 Greater PCF reached with assisted coughing can avert respiratory failure and, ultimately, delay or eliminate the need for tracheotomy for airway secretion removal.

Mechanical insufflation-exsufflation (MI-E) is a method for mechanically assisted coughing. MI-E involves a deep insufflation by a positive pressure blower followed immediately by a forced exsufflation in which high expiratory flow rates and a high expiratory pressure gradient are generated between the mouth and the alveoli. If the expiratory flow rates reached with MI-E can exceed those that can be produced during unassisted coughing and, in particular, exceed 2.7 L/s for patients with advanced neuromuscular ventilatory insufficiency,11 the risk of pulmonary complications can be diminished. While this has been demonstrated for patients with neuromuscular diseases with bulbar muscle function,5 it has not been demonstrated for bulbar ALS patients. Likewise, intubation, bronchoscopy, and tracheotomy for airway secretion expulsion may be avoided. The aim of this study, which constitutes a part of long-term prospective project whose objective is to evaluate the utility of noninvasive therapeutic procedures in ALS patients, is to determine under what circumstances MI-E is able to generate effective expiratory flow rates for medically stable patients with bulbar and nonbulbar ALS.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Twenty-six consecutively referred patients with ALS without antecedent lung disease or significant kyphoscoliosis (Cobb angle > 70°) were studied. The diagnosis of ALS was established by El Escorial criteria.12 Videofluoroscopy was performed of the upper airways, the capacity to perform a Valsalva maneuver was determined, and the presence of drooling or articulation difficulties was surveyed in order to estimate bulbar impairment.13 Bulbar dysfunction was considered when at least one of the previous alterations were present.13 Exclusion criteria were antecedent barotrauma, pulmonary bullae, or FEV1/FVC < 70%. Informed consent was obtained from each subject who took part in the study. All subjects were medically stable for at least 1 month. All measurements were made while the subjects were seated. Spirometry was performed (MS 2000; C. Schatzman; Madrid, Spain) using a mouthpiece and a nose clip. FVC, FEV1, and FVE1/FVC were recorded in accordance with European Respiratory Society guidelines and suggested normal values.14

Maximum inspiratory pressure (PImax) and maximum expiratory pressure (PEmax) at the mouth were measured (Electrometer 78.905A; Hewlett-Packard; Andover, MA) with cheek held. PImax was performed close to residual volume and PEmax was performed close to total lung capacity, and the pressures sustained for 1 s were observed. Three measurements with < 5% variability were recorded, and the highest value was used for the data analysis. Reference values were those of Morales et al.15

PCF were measured using a sealed oronasal mask (King Mask; King System; Noblesville, IN) connected to a pneumotachograph spirometer (MS 2000; C. Schatzman) when the subjects performed a maximal cough effort after a deep inspiration. MIC was attained using a manual resuscitator (Revivator; Hersill; Madrid, Spain) via a sealed oronasal mask (King Mask; King System). The lungs were insufflated to the highest volume that could be held with a closed glottis. The patient was then asked to cough forcefully while a thoracoabdominal thrust was applied. The cough volume and the PCF attained with the MIC (PCFMIC) were measured with a pneumotachograph connected to the mask and the manual resuscitator.

The MI-E (Cough-Assist; JH Emerson; Cambridge, MA) was applied through a full face mask (King Mask; King System). It was set at 40 cm H2O of insufflation pressure, – 40 cm H2O of exsufflation pressure with an insufflation/exsufflation ratio of 2/3, and a pause of 1 s between each cycle.722 The patient was asked to try to keep his airway open but to otherwise remain passive and let the Cough-Assist device act unimpeded on the airways. A thoracoabdominal thrust was applied during exsufflation to further increase the PCF.9 With a pneumotachograph placed between the mask and the MI-E circuit, PCF generated by MI-E (PCFMI-E) was measured.

Statistical Analysis
Data were expressed as mean ± SD. Data comparisons were performed by Student’s paired and unpaired t tests. When the variables did not have a normal distribution, the Mann Whitney test and Wilcoxon test for paired data were used. Receiver operating characteristic (ROC) curves were used in order to identify variables that would best predict those ALS patients for whom MI-E would probably be ineffective (PCFMI-E < 2.7 L/s)4 and those in whom manually assisted coughing would reach greater PCF than MI-E. The level for statistical significance was taken as p < 0.05.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Data for age, sex, pulmonary function, and cough capacity are shown in Table 1 . No differences were found between nonbulbar and bulbar patients over the period of time since ALS symptom onset (24.75 ± 12.91 months vs 30.70 ± 18.28 months, p = not significant), and in time from establishment of the diagnosis (18.44 ± 13.33 months vs 21.70 ± 16.34 months, p = not significant). Statistical differences (p < 0.05) were found in lung function and cough capacity parameters between bulbar and nonbulbar patients (Table 1).


View this table:
[in this window]
[in a new window]

  		Table 1.. Lung Function and Cough Capacity Parameters in the Subjects*

 
Twenty-four patients (92.31%) had MIC greater than FVC (MIC vs FVC, p < 0.01). Two patients who could not close their glottises had MIC values equal to FVC (1.11 ± 0.62 L) [mean ± SD]. Both of them also had severe bulbar dysfunction. All the patients with some degree of bulbar dysfunction and MIC greater than FVC were able to obtain a PCFMIC > 2.7 L/s except for one patient (FVC, 0.60 L; MIC, 1.01 L; PCF, 1.87 L/s; PCFMIC, 1.91 L/s). This patient (stable clinically but who had rejected tracheostomy as a means to clear secretions if needed) was probably able to close the glottis enough to increase the MIC, but his expiratory muscles were too weak (PEmax 35.5% of predicted value) to generate an adequate PCFMIC.

Seven patients had PCF < 2.7 L/s (2.25 ± 0.34 L/s), all of them with bulbar dysfunction. All of them had rejected tracheostomy as mean to clear secretions and/or mechanical ventilation if needed. Comparing these patients (PCF < 2.7 L/s) with those with PCF >= 2.7 L/s, we found that they presented lower PCFMIC (2.80 ± 0.30 L/s vs 5.95 ± 2.24 L/s, p < 0,001) and PCFMI-E (2.79 ± 0.38 L/s vs 4.12 ± 0.80 L/s, p < 0.001).

MI-E was able to generate PCFMI-E > 2.7 L/s in all but four patients (2.55 ± 0.09 L/s). A ROC curve was performed in order to seek variables that might predict the patients in whom the MI-E would be ineffective (PCFMI-E < 2.7 L/s). Of all the analyzed variables, PCFMIC had the greatest (p < 0.05) area under the curve (0.98; p < 0.01; 95% confidence interval, 0.82 to 0.99). A value of 2.7 L/s as cutoff point for the PCFMIC had a sensitivity of 1.00 and a specificity of 0.95 in identifying those patients with ineffective PCFMI-E for mucus clearance (< 2.7 L/s), with a positive predictive value of 0.79 and negative predictive value of 1.00. All these four patients have bulbar dysfunction, MIC > 1 L, and PCFMIC < 2.7 L/s.

Statistical differences (p < 0.05) were found between patients with PCFMI-E > 2.7 L/s (n = 22) and those with PCFMI-E < 2.7 L/s (n = 4) in PCF (4.85 ± 2.32 L/s vs 2.18 ± 0.45 L/s), PCFMIC (5.60 ± 2.26 L/s vs 2.29 ± 0.40 L/s), PCFMI-E (3.97 ± 0.82 L/s vs 2.55 ± 0.01 L/s), and PEmax (108.20 ± 70.21 cm H2O vs 60.75 ± 10.90 cm H2O).

A ROC curve was used in the patients we studied in order to seek variables that might predict medically stable patients for whom PCFMIC would be greater than PCFMI-E. The PCFMIC had the greatest area under the curve (0.90; p < 0.01; 95% confidence interval, 0.71 to 0.98). A value of 4 L/s as cutoff point for the PCFMIC had a sensitivity of 0.89 and a specificity of 0.75 in identifying patients with PCFMIC greater than PCF, with a positive predictive value of 0.68 and a negative predictive value of 0.93.

All the patients with no clinically relevant impairment in cough capacity (PCF >= 4.5 L/s)5 [n = 11, PCF, 6.45 ± 2.12 L/s; 4 patients with some degree of bulbar dysfunction] had MIC greater than FVC (3.13 ± 1.16 L vs 2.84 ± 1.16 L, p < 0.01). Moreover, in these patients PCFMIC was greater than PCFMI-E (7.01 ± 2.29 L/s vs 4.31 ± 0.92 L/s, p < 0.01).


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The most important findings in this study are the usefulness of the MI-E in ALS patients, both bulbar and nonbulbar, the critical role played by the upper airway in the generation of an effective mechanically assisted PCF, and the inability of MI-E to generate greater PCF than those attainable by manually assisted coughing alone for those medically stable patients with milder respiratory dysfunction. In these patients, we can assume that those with PCFMIC > 4 L/s may be unable to generate greater cough flows with the MI-E than manually assisted coughing. This work also demonstrates that inability to close the glottis and airway collapse are distinct factors in determining PCF and the potential effectiveness of MI-E.

Impaired cough capacity is a progressive state found in patients with ALS. The different degree of the involvement in the respiratory and bulbar muscles determines the success of the different assisted-coughing techniques in order to generate an effective PCF to remove airway secretions. Inspiratory muscle weakness produces a diminution of vital capacity and lung recoil pressures, expiratory muscle weakness produces a reduction in the intrathoracic pressure generated during the cough maneuver, and severe bulbar dysfunction with failure to close the glottis reduces or eliminates MIC, decreasing potential lung recoil for an effective cough. The result is a decreased PCF, more evident in bulbar patients, as our findings show. We also found that in those patients with ALS and expiratory and inspiratory muscle weakness but effective bulbar muscles, in order to close the glottis (MIC greater than FVC), the generated PCF with manually assisted coughing is greater than unassisted PCF (p < 0.01). This can change an ineffective cough into an effective one.1016 Indeed, the findings of our study show that in those patients with ALS and milder respiratory dysfunction and effective bulbar muscles, the generated PCFMIC is greater than those reached with MI-E. In this way, patients with MIC greater than FVC and PCFMIC > 4 L/s present PCFMIC greater than PCFMI-E in a stable condition. However, our results do not show what may happen to these same patients in an acute respiratory illness when they have airway secretions—for instance a pulmonary infection—when PCFMI-E would be more effective, and thereby more useful, than PCFMIC in order to airway secretions removal.17 Moreover, this study was conducted applying MI-E with a thoracoabdominal thrust and without any patient cough effort because we wanted to evaluate the peak expiratory flow rates generated by MI-E without patient cooperation. We performed our study thus because it is possible that in very advanced ALS or in situations in which no cooperation will be produced, no cough attempts will be made.17 However, the patient cough effort, a thoracoabdominal thrust during the exsufflation cycle, and probably greater set pressures in the MI-E will increase the PCFMI-E.91819

When manually assisted coughing techniques are unable to generate an effective PCF or when the patient is unable to cooperate, the MI-E is the most effective alternative for generating optimal PCF and eliminating airway secretions.9 In this way, the values of PCFMI-E recorded in our study are similar to those attained in previous clinical182021 and experimental studies.22 The findings of our study show that MI-E is able to generate a PCF > 2.7 L/s in patients with ALS when it is applied via a full face mask for patients both with and without bulbar dysfunction, except for those with severe bulbar dysfunction, MIC > 1 L, and PCFMIC < 2.7 L/s. This fact (MIC > 1 L and manually assisted PCF < 2.7 L/s) means that there is an alteration in the upper airway such as greater instability and weakness these muscles due to bulbar dysfunction.23 Because of a suspected upper airway collapse during the application of negative pressure, an upper airway CT scan was performed (Dr. M. A. Moya) at baseline and during the exsufflation cycle of MI-E for a patient whose PCFMI-E was < 2.7 L/s (PCFMI-E of 2.55 L/s), and for another patient with bulbar dysfunction and PCFMI-E > 2.7 L/s (PCFMI-E of 3 L/s), and for a nonbulbar patient with PCFMI-E > 2.7 L/s (PCFMI-E of 5.27 L/s). The upper airway CT scans of the three patients showed exsufflation cycle closing of the nasopharynx, with retraction of the uvula, and reduction of the lateral diameter of the pharynx. This narrowing was greatest at the oropharynx (Fig 1, 2 ). In the patient with PCFMI-E < 2.7 L/s, the maximum reduction of the diameter of the pharynx was 77%; in the patient with bulbar dysfunction and PCFMI-E > 2.7 L/s, it was 60%; and in the patient without bulbar impairment and PCFMI-E > 2.7 L/s, it was 45%.



View larger version (94K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1.. Oropharynx CT scan of a bulbar ALS patient with PCFMI-E < 2.7 L/s. Left, A: baseline. Right, B: during the exsufflation cycle.

 


View larger version (69K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 2.. Oropharynx CT scan of a nonbulbar ALS patient with PCFMI-E > 2.7 L/s. Left, A: baseline. Right, B: during the exsufflation cycle.

 
Koulouris et al24 proposed the application of negative pressure during tidal expiration (NEP) [– 3 to –5 cm H2O] in order to assess expiratory flow limitation. The sudden application of a NEP in healthy subjects produces reflex activation of the genioglossus muscle to maintain upper airway patency25 and prevent decreases in expiratory flow. If greater NEP is applied, the response of the genioglossus muscle reflex will be greater.26 Decreases in expiratory flow have also been demonstrated in healthy subjects when a NEP is applied, reflecting a total or partial narrowing of the upper airway, and suggesting some degree of upper airway instability.272829 This collapse of the upper airway during the application of NEP that is produced in certain healthy subjects can be due to too long a latency of the pharyngeal dilator muscle reflex or interindividual variations in the sensitivity of the trigger or in the intensity of response.25 Patients with ALS and impaired bulbar function have weakness of the pharyngeal muscles13 and, as in other neuromuscular disorders with bulbar dysfunction, the pharyngeal muscles have decreased strength, muscle velocity, and mechanical power.30 This fact can produce a diminution of the genioglossus muscle response when a NEP is applied, and produce a narrowing of the upper airway with a decrease in expiratory flows. In this way, the application of the exsufflation cycle of MI-E for those with weakness of genioglossus activity due to bulbar dysfunction would probably produce a dynamic, total, or partial collapse of the upper airway. This can render PCFMI-E ineffective.

The importance of the oropharyngeal musculature has been recognized for the generation of assisted PCF.16 Our study has permitted the identification of two not mutually exclusive circumstances in the bulbar ALS population: those with failure to close the glottis (MIC equal to FVC, and inability to perform a Valsalva maneuver), in whom manually assisted coughing cannot increase PCF; and those with instability of the pharyngeal walls (PCFMIC < 2.7 L/s and MIC > 1 L), in whom the MI-E is ineffective. One study7 has found that assisted coughing techniques tend to fail in patients with ALS and severe bulbar dysfunction, and tracheotomy becomes necessary to prolong survival. Moreover, bulbar onset has been related to poor survival.31 Consequently, we propose periodic monitoring of assisted coughing effectiveness (PCFMIC and PCFMI-E) in order to identify those patients at risk of failure of noninvasive management.

In conclusion, MI-E does not generate greater PCF than manually assisted coughing in those medically stable ALS patients with relatively little lung function impairment (PCFMIC > 4L/s), but it is able to significantly increase PCF > 2.7 L/s for patients both with and without bulbar dysfunction, except for those with bulbar dysfunction who also have a MIC > 1 L and PCFMIC < 2.7 L/s, probably due to dynamic collapse of the upper airway during the exsufflation cycle.


   Acknowledgements
 
The authors thank Dr. John R. Bach and Dr. Edward A. Oppenheimer for their helpful review of this manuscript.


   Footnotes
 
Abbreviations: ALS = amyotrophic lateral sclerosis; MIC = maximum insufflation capacity; MI-E = mechanical insufflation-exsufflation; NEP = negative pressure during tidal expiration; PCF = peak cough flow; PCFMI-E = peak cough flow generated by mechanical insufflation-exsufflation; PCFMIC = peak cough flow attained with maximum insufflation capacity; PEmax = maximum expiratory pressure; PImax = maximum inspiratory pressure; ROC = receiver operating characteristic

The preliminary results of this study were presented at the IX Congress of the Sociedad Valenciana de Neumología, Oliva, Spain, April 2002, and received the award for the best poster presentation.

Received for publication March 31, 2003. Accepted for publication September 1, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Schiffman, PL, Blesh, JM (1993) Pulmonary function at diagnosis of amyotrophic lateral sclerosis: rate of deterioration. Chest 103,508-513[Abstract/Free Full Text]
  2. Lechtzin, N, Wiener, CM, Clawson, MSN, et al Hospitalization in amyotrophic lateral sclerosis: causes, costs and outcomes. Neurology 2001;56,753-757[Abstract/Free Full Text]
  3. King, M, Brock, G, Lundell, C Clearance of mucus by simulated cough. J Appl Physiol 1985;58,1776-1782[Abstract/Free Full Text]
  4. Bach, JR, Saporito, LR Criteria for extubation and tracheostomy tube removal for patients with ventilatory failure: a different approach to weaning. Chest 1996;110,1566-1571[Abstract/Free Full Text]
  5. Bach, JR, Ishikama, Y, Kim, H Prevention of pulmonary morbidity for patients with Duchenne muscular dystrophy. Chest 1997;112,1024-1028[Abstract/Free Full Text]
  6. Poponick, JM, Jacobs, I, Supinski, G, et al Effect of upper respiratory tract infection in patients with neuromuscular disease. Am J Respir Crit Care Med 1997;156,659-664[Abstract/Free Full Text]
  7. Bach, JR Amyotrophic lateral sclerosis: prolongation of life by noninvasive respiratory aids. Chest 2002;122,92-98[Abstract/Free Full Text]
  8. Bach, JR, Alba, AS, Saporito, LR Intermittent positive pressure ventilation via the mouth as an alternative to tracheostomy for 257 ventilator users. Chest 1993;103,174-182[Abstract/Free Full Text]
  9. Bach, JR Mechanical insufflation-exsufflation: comparison of peak expiratory flows with manually assisted and unassisted coughing techniques. Chest 1993;104,1553-1562[Abstract/Free Full Text]
  10. Kang, SW, Bach, JR Maximum insufflation capacity: vital capacity and cough flows in neuromuscular disease. Am J Phys Med Rehabil 2000;79,222-227[Medline]
  11. Bach, JR, Smith, WH, Michaels, J, et al Airway secretion clearance by mechanical exsufflation for post-poliomyelitis ventilator assisted individual. Arch Phys Med Rehabil 1993;74,170-177[ISI][Medline]
  12. World Federation of Neurology Research Group on neuromuscular disease, subcommittee on motor neuron disease. El Escorial World Federation on Neurology Criteria for the Diagnosis of Amyotrophic Lateral Sclerosis. J Neurol Sci 1994;124,96-107
  13. Hadjikoutis, S, Wiles, CM Respiratory complications related to bulbar dysfunction in motor neuron disease. Acta Neurol Scand 2001;103,207-213[CrossRef][ISI][Medline]
  14. Quanjer, PhD, Tammeling, GJ, Cotes, JE, et al Lung volumes and forced ventilatory flows: report of Working Party "Standardization of Lung Function Test." Eur Respir J 1993;6(suppl 16),5-40
  15. Morales, P, Sanchis, J, Cordero, PJ, et al Presiones respiratorias estáticas máximas en adultos: valores de referencia en la población caucasiana mediterránea. Arch Bronconeumol 1997;33,213-219[Medline]
  16. Kang, SW, Bach, JR Maximum insufflation capacity. Chest 2000;118,61-65[Abstract/Free Full Text]
  17. Servera, E, Sancho, J, Gómez-Merino, E, et al Noninvasive management of an acute chest infection for a patient with ALS. J Neurol Sci 2003;209,11-13
  18. Barach, AL, Beck, GJ, Bickerman, HA, et al Physical methods simulating mechanism of the human cough. J Appl Physiol 1952;5,85-91[Free Full Text]
  19. Braun, SR, Giovannoni, R, O’Connor, M Improving the cough in patients with spinal cord injury. Am J Phys Med Rehabil 1984;63,1-10
  20. Chatwin, M, Ross, E, Hart, N, et al A comparison of the effect of mechanical insufflation-exsufflation, noninvasive ventilation and physiotherapy assistance on peak cough flow in neuromuscular disease. Thorax 2001;56(suppl 3),48-49[CrossRef]
  21. Mustfa, N, Aiello, M, Lyall, RA, et al Cough augmentation in bulbar and non-bulbar motor neuron disease patients [abstract]. Thorax 2001;56(suppl 3),49
  22. Gómez-Merino, E, Sancho, J, Marín, J, et al Mechanical insufflation-exsufflation: pressure, volume and flow relationships and the adequacy of the manufacturer’s guidelines. Am J Phys Med Rehabil 2002;81,579-583[Medline]
  23. Bach, JR, Tzeng, A, Servera, E Ayudas de medicina física en la prevención de morbilidad y mortalidad de los pacientes con enfermedades neuromusculares. Giménez, M Servera, E Vergara, P eds. Prevención y rehabilitación en patología respiratoria crónica 2001,421-430 Panamericana. Madrid, Spain:
  24. Koulouris, NG, Valta, P, Lavoice, A, et al A simple method to detect expiratory flow limitation during spontaneous breathing. Eur Respir J 1995;8,306-313[Abstract]
  25. Tantucci, C, Mehiri, S, Dugnet, A, et al Application of negative expiratory pressure during expiration and activity of genioglossus in humans. J Appl Physiol 1998;84,1076-1082[Abstract/Free Full Text]
  26. Horner, RL, Innes, JA, Guz, A Reflex pharyngeal dilator muscle activation by stimuli of negative airway pressure in awake man. Sleep 1993;16(suppl),S85-S86
  27. Suratt, PM, Wilhoit, SC, Cooper, K Induction of airway collapse with subatmospheric pressure in awake patients with sleep apnea. J Appl Physiol 1984;57,140-146[Abstract/Free Full Text]
  28. Sanna, A, Veriter, C, Kurtansky, A, et al Contraction and relaxation of upper airway muscles during expiratory application of negative pressure at the mouth. Sleep 1994;17,220-225[ISI][Medline]
  29. Younes, M, Sanii, R, Patrick, W, et al An approach to the study of upper airway function in humans. J Appl Physiol 1994;77,1383-1392[Abstract/Free Full Text]
  30. Attal, P, Lambert, F, Marchand-Adam, S, et al Severe mechanical dysfunction in pharyngeal muscle from adult mdx mice. Am J Respir Crit Care Med 2000;162,278-281[Abstract/Free Full Text]
  31. Magnus, T, Beck, M, Giess, R, et al Disease progression in amyotrophic lateral sclerosis: predictors of survival. Muscle Nerve 2002;25,709-714[CrossRef][ISI][Medline]



This article has been cited by other articles:


Home page
 ChestHome page
A. Ozsancak, C. D'Ambrosio, and N. S. Hill
Nocturnal Noninvasive Ventilation
Chest, May 1, 2008; 133(5): 1275 - 1286.
[Abstract] [Full Text] [PDF]

Home page
 ChestHome page
B. Fauroux, N. Guillemot, G. Aubertin, N. Nathan, A. Labit, A. Clement, and F. Lofaso
Physiologic Benefits of Mechanical Insufflation-Exsufflation in Children With Neuromuscular Diseases
Chest, January 1, 2008; 133(1): 161 - 168.
[Abstract] [Full Text] [PDF]

Home page
 ChestHome page
E. Servera and J. Sancho
Appropriate Management of Respiratory Problems Is of Utmost Importance in the Treatment of Patients With Amyotrophic Lateral Sclerosis
Chest, June 1, 2005; 127(6): 1879 - 1882.
[Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (21)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Sancho, J.
Right arrow Articles by Marín, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Sancho, J.
Right arrow Articles by Marín, J.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS