Airway clearance techniques in neuromuscular disorders: A state of the art review
Open accessAbstract
This is a unique state of the art review written by a group of 21 international recognized experts in the field that gathered during a meeting organized by the European Neuromuscular Centre (ENMC) in Naarden, March 2017. It systematically reports the entire evidence base for airway clearance techniques (ACTs) in both adults and children with neuromuscular disorders (NMD). We not only report randomised controlled trials, which in other systematic reviews conclude that there is a lack of evidence base to give an opinion, but also include case series and retrospective reviews of practice. For this review, we have classified ACTs as either proximal (cough augmentation) or peripheral (secretion mobilization). The review presents descriptions; standard definitions; the supporting evidence for and limitations of proximal and peripheral ACTs that are used in patients with NMD; as well as providing recommendations for objective measurements of efficacy, specifically for proximal ACTs. This state of the art review also highlights how ACTs may be adapted or modified for specific contexts (e.g. in people with bulbar insufficiency; children and infants) and recommends when and how each technique should be applied.
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Normal trans tracheal suctioning with a catheter is not completely effective in more than 90% of cases and peripheral secretions are not removed.
“As shown by Chatwin, normal trans tracheal suctioning with a catheter is not completely effective in more than 90% of cases and thus peripheral secretions are not removed [52].”
From Life Experiences in Neuromuscular Tracheotomized Patients in Times of Covid-19 (2023) · cites this paper as [52]
Section 3.3.2.3 (page unavailable) says routine catheter suctioning does not directly remove secretions from peripheral airways. It does not report that suctioning is incompletely effective in more than 90% of cases; searches for that percentage found no supporting passage. (LLM, conf=0.88)
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Self-citationProlonging Survival in Amyotrophic Lateral Sclerosis
Sancho, J., Servera, E., Bañuls, P., & Marín, J. (2010) · American Journal of Physical Medicine & Rehabilitation · doi:10.1097/phm.0b013e3181d8a479 · Cited by 29 · see citing works
Self-citationMoran, F. C., Spittle, A. J., & Delany, C. M. (2014) · Respiratory Care · doi:10.4187/respcare.03641 · Cited by 29 · see citing works
Toussaint, M., Guillet, M.-C., Paternotte, S., Soudon, P., & Haan, J. (2011) · Respiratory Care · doi:10.4187/respcare.01441 · Cited by 28 · see citing works
Self-citationHov, B., Andersen, T. M., Hovland, V., & Toussaint, M. (2017) · Paediatric Respiratory Reviews · doi:10.1016/j.prrv.2017.08.003 · Cited by 26 · see citing works
Self-citationIndications de la ventilation à percussions intrapulmonaires (VPI) : revue de la littérature
Riffard, G., & Toussaint, M. (2012) · Revue des Maladies Respiratoires · doi:10.1016/j.rmr.2011.12.005 · Cited by 25 · see citing works
Self-citationBreath stacking in children with neuromuscular disorders
Jenkins, H. M., Stocki, A., Kriellaars, D. J., & Pasterkamp, H. (2013) · Pediatric Pulmonology · doi:10.1002/ppul.22865 · Cited by 25 · see citing works
Use of a lung model to assess mechanical in‐exsufflator therapy in infants with tracheostomy
Striegl, A. M., Redding, G. J., DiBlasi, R. M., Crotwell, D. N., Salyer, J. W., & Carter, E. R. (2010) · Pediatric Pulmonology · doi:10.1002/ppul.21353 · Cited by 25 · see citing works
Bianchi, C. M., Carrara, R., Khirani, S., & Tuccio, M. C. (2013) · American Journal of Physical Medicine & Rehabilitation · doi:10.1097/phm.0b013e3182975bfa · Cited by 25 · see citing works
Bidiwala, A., Volpe, L., Halaby, C., Fazzari, M. J., Valsamis, C., & Pirzada, M. B. (2016) · Postgraduate Medicine · doi:10.1080/00325481.2017.1264854 · Cited by 24 · see citing works
Sarmento, A., Resqueti, V., Júnior, M. E. T. D., da Silva, L. S., Aliverti, A., Fregonezi, G., & de Andrade, A. D. (2017) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2017.04.015 · Cited by 24 · see citing works
Rutkowski, A., Chatwin, M., Koumbourlis, A. C., Fauroux, B., & Simonds, A. K. (2014) · Neuromuscular Disorders · doi:10.1016/j.nmd.2014.11.003 · Cited by 22 · see citing works
Self-citationExperiences with using mechanical in–exsufflation in amyotrophic lateral sclerosis
Siewers, V., Holmøy, T., & Frich, J. C. (2013) · European Journal of Physiotherapy · doi:10.3109/21679169.2013.834513 · Cited by 21 · see citing works
Measurement of Cough Aerodynamics in Healthy Adults
Feinstein, A. J., Zhang, Z., Chhetri, D. K., & Long, J. L. (2017) · Annals of Otology Rhinology & Laryngology · doi:10.1177/0003489417694912 · Cited by 21 · see citing works
Keating, J. M., Collins, N., Bush, A., & Chatwin, M. (2011) · Respiratory Care · doi:10.4187/respcare.01155 · Cited by 19 · see citing works
Self-citationEffects of restricted thoracic movement on the regional distribution of ventilation
Pulletz, S., Elke, G., Zick, G., Schädler, D., Reifferscheid, F., Weiler, N., & Frerichs, I. (2010) · Acta Anaesthesiologica Scandinavica · doi:10.1111/j.1399-6576.2010.02233.x · Cited by 18 · see citing works
Management of Oropharyngeal and Tracheobronchial Secretions in Patients with Neurologic Disease
Elman, L. B., Dubin, R. M., Kelley, M., & McCluskey, L. F. (2005) · Journal of Palliative Medicine · doi:10.1089/jpm.2005.8.1150 · Cited by 17 · see citing works
Glossopharyngeal pistoning for lung insufflation in children with spinal muscular atrophy type II
Nygren‐Bonnier, M., Markström, A., Lindholm, P., Mattsson, E., & Klefbeck, B. (2009) · Acta Paediatrica · doi:10.1111/j.1651-2227.2009.01343.x · Cited by 17 · see citing works
Self-citationCrescimanno, G., & Marrone, O. (2010) · Revista Portuguesa de Pneumologia · doi:10.1016/s0873-2159(15)31254-x · Cited by 15 · see citing works
Acute effects of glossopharyngeal insufflation in people with cervical spinal cord injury
Nygren‐Bonnier, M., Schiffer, T. A., & Lindholm, P. (2017) · Journal of Spinal Cord Medicine · doi:10.1080/10790268.2016.1275446 · Cited by 11 · see citing works
Self-citationChanges in gastric pressure and volume during mechanical in‐exsufflation
Miske, L. J., McDonough, J. M., Weiner, D. J., & Panitch, H. B. (2012) · Pediatric Pulmonology · doi:10.1002/ppul.22671 · Cited by 9 · see citing works
Nygren‐Bonnier, M., Werner, J., Biguet, G., & Johansson, S. (2017) · Disability and Rehabilitation · doi:10.1080/09638288.2017.1304583 · Cited by 9 · see citing works
Self-citationRiffard, G., Buzenet, J., & Guérin, C. (2013) · Respiratory Care · doi:10.4187/respcare.02727 · Cited by 8 · see citing works
Léger, P., & Paulus, J. (2006) · PubMed · Cited by 8 · see citing works
Travlos, V., Drew, K., & Patman, S. M. (2014) · Developmental Neurorehabilitation · doi:10.3109/17518423.2014.993771 · Cited by 7 · see citing works
Assessment of gas compression and lung volume during air stacking maneuver
Sarmento, A., Resqueti, V., Fregonezi, G., & Aliverti, A. (2016) · European Journal of Applied Physiology · doi:10.1007/s00421-016-3511-y · Cited by 7 · see citing works
Kinésithérapie respiratoire instrumentale chez l’enfant neurologique central
Toussaint, M., Pernet, K., & Stagnara, A. (2015) · Motricité Cérébrale · doi:10.1016/j.motcer.2015.03.003 · Cited by 5 · see citing works
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Research works printed but not linked: 1
- G. Riffard, M. Toussaint, Indications for intrapulmonary percussive ventilation (IPV): a review of the literature, Rev. Mal. Respir. 29 (2) (2012) 178-190.
Cited by
Sorted by citations
Respiratory Management of Patients With Neuromuscular Weakness
Khan, A., Frazer-Green, L., Amin, R., Wolfe, L. F., Faulkner, G. G., II, Casey, K. R., Sharma, G. D., Selim, B. J., Zielinski, D., Aboussouan, L. S., et al. (2023) · CHEST Journal · doi:10.1016/j.chest.2023.03.011 · Cited by 144 · see citing works
Airway Clearance Techniques: The Right Choice for the Right Patient
Belli, S., Prince, I., Savio, G., Paracchini, E., Cattaneo, D., Bianchi, M., Masocco, F., Bellanti, M. T., & Balbi, B. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.544826 · Cited by 111 · see citing works
“There are precise guidelines on the use of cough assist treatment in patients with NMD (45), while it has not been found to be very effective in patients with COPD (46).”
BackgroundBTS clinical statement on aspiration pneumonia
Simpson, A. J., Allen, J.-L., Chatwin, M., Crawford, H., Elverson, J., Ewan, V. C., Forton, J. T., McMullan, R., Plevris, J. N., Renton, K., et al. (2023) · Thorax · doi:10.1136/thorax-2022-219699 · Cited by 104 · see citing works
Self-citationChatwin, M., & Simonds, A. K. (2019) · Respiratory Care · doi:10.4187/respcare.06882 · Cited by 93 · see citing works
Self-citationNIV in amyotrophic lateral sclerosis: The ‘when’ and ‘how’ of the matter
Morélot‐Panzini, C., Bruneteau, G., & Gonzalez‐Bermejo, J. (2019) · Respirology · doi:10.1111/resp.13525 · Cited by 89 · see citing works
Intensive Care and Treatment of Severe Guillain–Barré Syndrome
Shang, P., Feng, J., Wu, W., & Zhang, H. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.608130 · Cited by 75 · see citing works
“Airway clearance strategies including assisted cough or air stacking and appropriate antibiotic therapy attenuate morbidity of HAP/VAP in GBS cohorts (Koenig and Truwit, 2006; Chatwin et al., 2018).”
BackgroundLegg, J. P., Allen, J.-L., Andrew, M., Annesley, C., Chatwin, M., Crawford, H., Elverson, J., Forton, J. T., Oulton, K., Renton, K., et al. (2023) · Thorax · doi:10.1136/thorax-2022-219698 · Cited by 75 · see citing works
Self-citationNon-invasive ventilation in amyotrophic lateral sclerosis
Dorst, J., & Ludolph, A. C. (2019) · Therapeutic Advances in Neurological Disorders · doi:10.1177/1756286419857040 · Cited by 74 · see citing works
Practical approach to respiratory emergencies in neurological diseases
Racca, F., Vianello, A., Mongini, T., Ruggeri, P., Versaci, A., Vita, G. L., & Vita, G. (2019) · Neurological Sciences · doi:10.1007/s10072-019-04163-0 · Cited by 74 · see citing works
Laryngeal Responses to Mechanically Assisted Cough in Progressing Amyotrophic Lateral Sclerosis
Andersen, T. M., Sandnes, A., Fondenes, O., Nilsen, R. M., Tysnes, O., Heimdal, J., Clemm, H. H., Halvorsen, T., Vollsæter, M., & Røksund, O. D. (2018) · Respiratory Care · doi:10.4187/respcare.05924 · Cited by 66 · see citing works
Self-citationRespiratory Involvement in Patients with Neuromuscular Diseases: A Narrative Review
Voulgaris, A., Antoniadou, M., Agrafiotis, M., & Steiropoulos, P. (2019) · Pulmonary Medicine · doi:10.1155/2019/2734054 · Cited by 61 · see citing works
Respiratory muscle training in neuromuscular disease: a systematic review and meta-analysis
Watson, K. A., Egerton, T., Sheers, N. L., Retica, S., McGaw, R., Clohessy, T. A., Webster, P., & Berlowitz, D. J. (2022) · European Respiratory Review · doi:10.1183/16000617.0065-2022 · Cited by 53 · see citing works
Self-citationCough augmentation techniques for people with chronic neuromuscular disorders
Morrow, B. M., Argent, A. C., Zampoli, M., Human, A., Corten, L., & Toussaint, M. (2021) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd013170.pub2 · Cited by 53 · see citing works
Self-citationMechanical Insufflation-Exsufflation: Considerations for Improving Clinical Practice
Chatwin, M., & Wakeman, R. H. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12072626 · Cited by 50 · see citing works
“This is repeated and the highest value is taken to be their CPF [5,8].”
BackgroundMethodInfluentialSelf-citationCurrent developments and future directions in respiratory physiotherapy
Rodrigues, A., Castro, G. M., Jácome, C. I. O., Langer, D., Parry, S. M., & Burtin, C. (2020) · European Respiratory Review · doi:10.1183/16000617.0264-2020 · Cited by 48 · see citing works
Patel, N., Chong, K., & Baydur, A. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.838414 · Cited by 59 · see citing works
“As a result, ineffective airway clearance predispose to recurrent pneumonia a major cause of mortality and morbidity (Chatwin et al., 2018).”
BackgroundProposals from a French expert panel for respiratory care in ALS patients
Georges, M., Perez, T., Rabec, C. A., Jacquin, L., Monnier, A., Ramos, C., Patout, M., Attali, V., Amador, M. D. M., Gonzalez‐Bermejo, J., et al. (2022) · Respiratory Medicine and Research · doi:10.1016/j.resmer.2022.100901 · Cited by 46 · see citing works
Long-Term Non-invasive Ventilation in Children: Current Use, Indications, and Contraindications
Praud, J.-P. (2020) · Frontiers in Pediatrics · doi:10.3389/fped.2020.584334 · Cited by 46 · see citing works
Building a home ventilation programme: population, equipment, delivery and cost
Toussaint, M., Wijkstra, P. J., Mckim, D. A., Benditt, J. O., Winck, J. C., Nasiłowski, J., & Borel, J. (2022) · Thorax · doi:10.1136/thoraxjnl-2021-218410 · Cited by 45 · see citing works
Self-citationUpper Airway Assessment and Responses During Mechanically Assisted Cough
Andersen, T. M., Hov, B., Halvorsen, T., Røksund, O. D., & Vollsæter, M. (2021) · Respiratory Care · doi:10.4187/respcare.08960 · Cited by 43 · see citing works
Self-citationRespiratory therapies for Amyotrophic Lateral Sclerosis: A state of the art review
Campos, P. F., Olsen, W. L., Wymer, J. P., & Smith, B. K. (2023) · Chronic Respiratory Disease · doi:10.1177/14799731231175915 · Cited by 42 · see citing works
“Cough is an important protective mechanism to clear excess secretions, irritants, and foreign matter from the airways.(17,18) As illustrated in Figure 2, generation of adequate cough requires a complex coordination of the inspiratory muscles for a deep inspiration, increasing lung volume, upper airway muscles for rapi…”
BackgroundThe optimisation of noninvasive ventilation in amyotrophic lateral sclerosis: a systematic review
O’Brien, D., Stavroulakis, T., Baxter, S. K., Norman, P. E., Bianchi, S. M., Elliott, M., Johnson, M., Clowes, M., García‐Sánchez, A., Hobson, E., et al. (2019) · European Respiratory Journal · doi:10.1183/13993003.00261-2019 · Cited by 38 · see citing works
“A recent review highlighted the broad range of airway clearance techniques available, which may be adapted according to individual patient requirements (77).”
BackgroundRespiratory adjuncts to NIV in neuromuscular disease
Sheers, N. L., Howard, M. E., & Berlowitz, D. J. (2018) · Respirology · doi:10.1111/resp.13431 · Cited by 37 · see citing works
Self-citationHansen-Flaschen, J. H., & Ackrivo, J. (2023) · Respiratory Care · doi:10.4187/respcare.10349 · Cited by 34 · see citing works
The Use of Mechanical Insufflation-Exsufflation in Invasively Ventilated Critically Ill Adults
Swingwood, E. L., Stilma, W., Tume, L. N., Cramp, F. L., Voss, S. E., Bewley, J., Ntoumenopoulos, G., Schultz, M. J., Reimer, W. J. M. S. O., Paulus, F., et al. (2022) · Respiratory Care · doi:10.4187/respcare.09704 · Cited by 33 · see citing works
“It is this rapid alternation between positive and negative-pressure breaths that augments gas flows, improves sputum mobilization, and ultimately stimulates a cough.(6) More recently, there has been growing interest of MI-E use for intubated critically ill adults.”
Lacombe, M., Boré, A., Castrillo, L. D. A., Boussaïd, G., Falaize, L., Vlachos, E., Orlikowski, D., Prigent, H., & Lofaso, F. (2019) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2019.06.012 · Cited by 31 · see citing works
Self-citationGonzález-Sánchez, M., Ramı́rez-Expósito, M. J., & Martı́nez-Martos, J. M. (2025) · Life · doi:10.3390/life15040647 · Cited by 30 · see citing works
“ALS intensely impairs day-to-day activities of daily living and health-related quality of life for both patients and caregivers [197,198].”
Childs, A., Turner, C. E., Astin, R., Bianchi, S. M., Bourke, J. P., Cunningham, V. J., Edel, L., Edwards, C., Farrant, P., Heraghty, J., et al. (2023) · Thorax · doi:10.1136/thorax-2023-220811 · Cited by 27 · see citing works
Respiratory failure and sleep-disordered breathing in late-onset Pompe disease: a narrative review
Shah, N. M., Sharma, L., Ganeshamoorthy, S., & Kaltsakas, G. (2020) · Journal of Thoracic Disease · doi:10.21037/jtd-cus-2020-007 · Cited by 27 · see citing works
“A wide array of secretion clearance techniques is available, depending upon whether the patient needs support in mobilising their secretions from distal to proximal airways, or expelling secretions from the proximal airways (79).”
BackgroundImproving Care and Empowering Adults Living with SMA: A Call to Action in the New Treatment Era
Walter, M. C., Chiriboga, C. A., Duong, T., Goemans, N., Mayhew, A. G., Ouillade, L., Oskoui, M., Quinlivan, R. C. M., Vazquez-Costa, J. F., Vissing, J., et al. (2021) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-200611 · Cited by 27 · see citing works
“improved respiratory care [5], home adaptations [6], and devices that allow for greater independence, such as power wheelchairs and voice amplifiers [7]).”
BackgroundSancho, J., Ferrer, S., Burés, E., Fernández-Presa, L., Bañuls, P., Gonzalez, M. C., & Signes‐Costa, J. (2022) · Respiratory Care · doi:10.4187/respcare.09978 · Cited by 27 · see citing works
“…graphics were analyzed without an image of upper airway during MI-E application, although we took previously described graphs as a reference 8,17,18 ; and trans-nasal fiberoptic laryngoscopy could interfere with the flows generated during MI-E sessions, whereas use of local anesthesia could…”
Self-citationFitzgerald, D. A., Doumit, M., & Abel, F. (2018) · Paediatric Respiratory Reviews · doi:10.1016/j.prrv.2018.07.002 · Cited by 27 · see citing works
Prolonged Mechanical Ventilation, Weaning, and the Role of Tracheostomy
Rose, L., & Messer, B. (2024) · Critical Care Clinics · doi:10.1016/j.ccc.2024.01.008 · Cited by 26 · see citing works
The role of lung volume recruitment therapy in neuromuscular disease: a narrative review
Sheers, N. L., O’Sullivan, R., Howard, M. E., & Berlowitz, D. J. (2023) · Frontiers in Rehabilitation Sciences · doi:10.3389/fresc.2023.1164628 · Cited by 27 · see citing works
Self-citationTerzi, N., Guérin, C., & Gonçalves, M. (2018) · Intensive Care Medicine · doi:10.1007/s00134-018-5484-2 · Cited by 26 · see citing works
Self-citationSpinou, A. (2020) · Physiological Research · doi:10.33549/physiolres.934407 · Cited by 26 · see citing works
Swingwood, E. L., Tume, L. N., & Cramp, F. L. (2019) · Journal of the Intensive Care Society · doi:10.1177/1751143719870121 · Cited by 25 · see citing works
“The rapidly alternating positive and negative pressure aims to produce airflow in the airway approximating a normal cough.(14) There are a number of MI-E devices available for use within the UK.”
BackgroundEffect of mechanical insufflation‐exsufflation in children with neuromuscular weakness
Veldhoen, E. S., den Oudenrijn, L. P. V., Ros, L. A. A., Hulzebos, E. H. J., Papazova, D. A., van der Ent, C. K., van der Pol, W. L., Nijman, J., & Asperen, R. M. W. (2020) · Pediatric Pulmonology · doi:10.1002/ppul.24614 · Cited by 25 · see citing works
Comparison of 6 Oscillatory Positive Expiratory Pressure Devices During Active Expiratory Flow
Poncin, W., Reychler, G., Liistro, M., & Liistro, G. (2019) · Respiratory Care · doi:10.4187/respcare.07271 · Cited by 24 · see citing works
Morrow, B. M., Angelil, L., Forsyth, J., Huisamen, A., Juries, E., & Corten, L. (2019) · South African Journal of Physiotherapy · doi:10.4102/sajp.v75i1.1296 · Cited by 23 · see citing works
“For an effective cough, one needs adequate inspiration to above 80% of total lung capacity, glottic closure and a coordinated active exhalation with maximal expiratory flows combined with expulsive glottis opening (Boitano 2006: 913–922; Chatwin et al. 2018:98–110).”
BackgroundMethodResultInfluentialSelf-citationGray, L. T., Vasilopoulos, T., & Plowman, E. K. (2020) · Muscle & Nerve · doi:10.1002/mus.27040 · Cited by 23 · see citing works
“evidence-based recommendations include cough augmentation and ventilatory support, which are recommended once impairments in airway clearance and respiration are determined.(15) However, bulbar interventions, such”
BackgroundPulmonary care for ALS : Progress, gaps, and paths forward
Ackrivo, J. (2023) · Muscle & Nerve · doi:10.1002/mus.27779 · Cited by 23 · see citing works
“There are several mechanisms for improving airway clearance in ALS even at earlier stages of disease when forced vital capacity (FVC) and PCF are mildly reduced.(22,23) These techniques are most”
BackgroundS2k-Leitlinie Nichtinvasive Beatmung als Therapie der akuten respiratorischen Insuffizienz
Westhoff, M., Neumann, P., Geiseler, J. G., Bickenbach, J., Arzt, M. E., Bachmann, M., Braune, S. A., Delis, S., Dellweg, D., Dreher, M., et al. (2023) · Pneumologie · doi:10.1055/a-2148-3323 · Cited by 22 · see citing works
Chatwin, M., Gonçalves, M., Gonzalez‐Bermejo, J., Toussaint, M., Toussaint, M., Chatwin, M., Gonzalez‐Bermejo, J., Gonçalves, M., Benditt, J. O., Mckim, D. A., et al. (2020) · Neuromuscular Disorders · doi:10.1016/j.nmd.2020.07.008 · Cited by 22 · see citing works
“MPV can be used as a proximal ACT [6 , 7] .”
InfluentialSelf-citationKatz, S. L., Mah, J. K., McMillan, H. J., Campbell, C., Bijelić, V., Barrowman, N., Momoli, F., Blinder, H., Aaron, S. D., McAdam, L. C., et al. (2022) · Thorax · doi:10.1136/thoraxjnl-2021-218196 · Cited by 22 · see citing works
Self-citationMcDonald, L. A., Berlowitz, D. J., Howard, M. E., Rautela, L., Chao, C., & Sheers, N. L. (2019) · Respirology Case Reports · doi:10.1002/rcr2.447 · Cited by 22 · see citing works
“Neuromuscular disease (NMD) often involves muscles of the respiratory system, and may result in ventilatory failure and increased risk of respiratory tract infection [1,2].”
BackgroundSelf-citationUrushitani, M., Warita, H., Atsuta, N., Izumi, Y., Kano, O., Shimizu, T., Nakayama, Y., Narita, Y., Nodera, H., Fujita, T., et al. (2024) · Rinsho Shinkeigaku · doi:10.5692/clinicalneurol.cn-001946 · Cited by 21 · see citing works
“ALS, amyotrophic lateral sclerosis; FVC, forced vital capacity; MAC, manually assisted cough; MI-E, mechanical insufflation-exsufflation, NIV, noninvasive ventilation; TIV, tracheostomy invasive ventilation; VTPCV, volume-targeted pressure-controlled ventilation.”
MethodInfluentialThe adult multidisciplinary respiratory neuromuscular clinic
Shah, N. M., Murphy, P. B., & Kaltsakas, G. (2020) · Breathe · doi:10.1183/20734735.0121-2020 · Cited by 21 · see citing works
“At a minimum, the respiratory NMD MDT should be staffed and equipped to be able to offer manual assisted coughs, mechanical insufflation–exsufflation, lung volume recruitment, glossopharyngeal breathing, and chest wall percussion and oscillation [59].”
MethodThe complexity of multidisciplinary respiratory care in amyotrophic lateral sclerosis
Berlowitz, D. J., Mathers, S., Hutchinson, K., Hogden, A., Carey, K. A., Graco, M., Whelan, B., Charania, S., Steyn, F. J., Allcroft, P., et al. (2023) · Breathe · doi:10.1183/20734735.0269-2022 · Cited by 21 · see citing works
Self-citationEstimation of Cough Peak Flow Using Cough Sounds
Umayahara, Y., Soh, Z., Sekikawa, K., Kawae, T., Otsuka, A., & Tsuji, T. (2018) · Sensors · doi:10.3390/s18072381 · Cited by 20 · see citing works
“Moreover, the complex device setup, including firmly attaching the facemasks and infection control filters on the patient [1], imposes burdens on both patients and their caregivers.”
BackgroundPennati, F., LoMauro, A., D’Angelo, M. G., & Aliverti, A. (2021) · Life · doi:10.3390/life11090947 · Cited by 20 · see citing works
“glossopharyngeal breathing or air stacking [115].”
BackgroundRespiratory considerations in patients with neuromuscular disorders
Patel, N., Howard, I. M., & Baydur, A. (2023) · Muscle & Nerve · doi:10.1002/mus.27845 · Cited by 20 · see citing works
“breaths taken without expiration (glottis acting as check valve) until maximum inspiratory capacity is achieved, thereby increasing lung elastic recoil.(91) Assisted breath stacking may be achieved with an”
BackgroundShah, N. M., Apps, C., Kaltsakas, G., Madden-Scott, S., Suh, E., D'Cruz, R. F., Arbane, G., Patout, M., Lhuillier, E., Hart, N., et al. (2023) · CHEST Journal · doi:10.1016/j.chest.2023.10.015 · Cited by 20 · see citing works
Chen, T., Liang, W., Chen, I., Liu, Y., Hsu, J., & Jong, Y. (2019) · Therapeutic Advances in Respiratory Disease · doi:10.1177/1753466619875928 · Cited by 20 · see citing works
Cough Effectiveness and Pulmonary Hygiene Practices in Patients with Pompe Disease
Pitts, T. E., Bordelon, R. C., Huff, A. D., Byrne, B. J., & Smith, B. K. (2018) · Lung · doi:10.1007/s00408-018-0171-1 · Cited by 19 · see citing works
“A facemask is preferred in patients with bulbar muscle involvement [28], and recent consensus guidelines recommend a facemask for PCF testing in neuromuscular disease [12].”
MethodHuguet-Rodríguez, M., Arias‐Buría, J. L., Huguet-Rodríguez, B., Blanco-Barrero, R., Braña-Sirgo, D., & Güeita‐Rodríguez, J. (2020) · Brain Sciences · doi:10.3390/brainsci10070458 · Cited by 18 · see citing works
“Obtaining a measurement in L/min, this measures determines the patient’s ability to perform a productive cough and is of great clinical importance [25,26].”
BackgroundSheers, N. L., Berlowitz, D. J., Dirago, R. K., Naughton, P., Henderson, S., Rigoni, A., Saravanan, K., Rochford, P. D., & Howard, M. E. (2022) · BMJ Open Respiratory Research · doi:10.1136/bmjresp-2022-001241 · Cited by 18 · see citing works
Self-citationEckerland, M., Bock, C., Olivier, M., Pichlmaier, L., Steindor, M., & Stehling, F. (2019) · ERJ Open Research · doi:10.1183/23120541.00149-2018 · Cited by 18 · see citing works
Airway clearance in patients with neuromuscular disease
Gipsman, A. I., Lapinel, N. C., & Mayer, O. H. (2023) · Paediatric Respiratory Reviews · doi:10.1016/j.prrv.2023.02.002 · Cited by 17 · see citing works
Characterizing Expiratory Respiratory Muscle Degeneration in Duchenne Muscular Dystrophy Using MRI
Barnard, A. M., Lott, D. J., Batra, A., Triplett, W. T., Willcocks, R. J., Forbes, S. C., Rooney, W. D., Daniels, M. J., Smith, B. K., Vandenborne, K., et al. (2021) · CHEST Journal · doi:10.1016/j.chest.2021.08.078 · Cited by 16 · see citing works
Long-term follow-up of respiratory function in facioscapulohumeral muscular dystrophy
Teeselink, S., Vincenten, S. C. C., Voermans, N. C., Groothuis, J. T., Doorduin, J., Wijkstra, P. J., Horlings, C. G. C., van Engelen, B. G. M., & Mul, K. (2022) · Journal of Neurology · doi:10.1007/s00415-022-10990-7 · Cited by 16 · see citing works
“This could be caused by (aerobic) exercising, weight loss, respiratory physiotherapy techniques [19] or better patient cooperation.”
BackgroundEdel, L., Grime, C., Robinson, V., Manzur, A. Y., Abel, F., Munot, P., Ridout, D. A., Scoto, M., Francesco Muntoni, A., & Chan, E. (2021) · Neuromuscular Disorders · doi:10.1016/j.nmd.2021.01.008 · Cited by 16 · see citing works
Veldhoen, E. S., Vercoelen, F., Ros, L. A. A., den Oudenrijn, L. P. V., Asperen, R. M. W., Hulzebos, E. H. J., Bartels, B., Gaytant, M. A., van der Ent, C. K., & van der Pol, W. L. (2022) · Chronic Respiratory Disease · doi:10.1177/14799731221094619 · Cited by 16 · see citing works
Gray, L. T., Donohue, C., Vasilopoulos, T., Wymer, J. P., & Plowman, E. K. (2023) · Journal of Speech Language and Hearing Research · doi:10.1044/2022_jslhr-22-00522 · Cited by 15 · see citing works
Sheers, N. L., Howard, M. E., Rochford, P. D., Rautela, L., Chao, C., Mckim, D. A., & Berlowitz, D. J. (2023) · Annals of the American Thoracic Society · doi:10.1513/annalsats.202212-1062oc · Cited by 16 · see citing works
“This improvement is similar to the gain of 154 ( 2 13 to 322) ml in LIC reported in a 3-month, prospective, uncontrolled study of 16 adults with ALS/MND, postpolio syndrome, or myotonic dystrophy (mean FVC, 60%pn) (27).”
InfluentialSelf-citationPeak Expiratory Flow During Mechanical Insufflation-Exsufflation: Endotracheal Tube Versus Face Mask
Hyun, S. E., Lee, S., & Shin, H. (2021) · Respiratory Care · doi:10.4187/respcare.09150 · Cited by 15 · see citing works
“…discomfort (eg, dyspnea, dizziness, nausea, worsening of gastro-oesophageal reflux, chest or abdominal discomfort) during or after MI-E therapy 4,15 and to report their satisfaction with the treatment using a 5-point Likert scale, from 1 ¼ very dissatisfied to 5 ¼ very satisfied, if they were…”
Chatwin, M., Sancho, J., Luján, M., Andersen, T. M., & Winck, J. C. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13092643 · Cited by 14 · see citing works
Self-citationHuman, A., & Morrow, B. M. (2021) · South African Journal of Physiotherapy · doi:10.4102/sajp.v77i1.1577 · Cited by 13 · see citing works
“Introduction Children with neuromuscular diseases (NMD) often present with respiratory morbidity because of underlying progressive respiratory muscle weakness (Chatwin et al. 2018; Mayer et al. 2017; Park et al. 2010).”
BackgroundSelf-citationVeldhoen, E. S., van der Wal, R., den Oudenrijn, L. P. V., Asperen, R. M. W., Gaytant, M. A., van der Ent, C. K., van der Pol, W. L., & Hulzebos, E. H. J. (2023) · Respiratory Care · doi:10.4187/respcare.09664 · Cited by 13 · see citing works
Swingwood, E. L., Stilma, W., Tume, L. N., Cramp, F. L., Paulus, F., Schultz, M. J., Reimer, W. J. M. S. O., & Rose, L. (2020) · Systematic Reviews · doi:10.1186/s13643-020-01547-8 · Cited by 13 · see citing works
Brekka, A. K., Vollsæter, M., Ntoumenopoulos, G., Clemm, H. H., Halvorsen, T., Røksund, O. D., & Andersen, T. M. (2022) · BMJ Open · doi:10.1136/bmjopen-2021-059234 · Cited by 13 · see citing works
Self-citationA prospective examination of swallow and cough dysfunction after lung transplantation
Dallal‐York, J., Croft, K., Anderson, A. S., DiBiase, L., Donohue, C., Vasilopoulos, T., Shahmohammadi, A., Peláez, A., Pipkin, M., Wheeler‐Hegland, K., et al. (2022) · Neurogastroenterology & Motility · doi:10.1111/nmo.14458 · Cited by 13 · see citing works
Optimizing expiratory flows during mechanical cough in a pediatric neuromuscular lung model
Hov, B., Andersen, T. M., Toussaint, M., Fondenes, O., Carlsen, K. C. L., & Hovland, V. (2019) · Pediatric Pulmonology · doi:10.1002/ppul.24606 · Cited by 13 · see citing works
Self-citationHov, B., Andersen, T. M., Toussaint, M., Vollsæter, M., Mikalsen, I. B., Indrekvam, S., & Hovland, V. (2021) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.14797 · Cited by 13 · see citing works
Self-citationSansone, V., Proserpio, P., Mauro, L., Biostat, A. L., Frezza, E., Lanza, A., Rogliani, P., Pezzuto, G., Falcier, E., Aggradi, C. R. F., et al. (2021) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.9438 · Cited by 12 · see citing works
“29 The best value was recorded.”
Self-citationFactors associated with extubation failure in an intensive care unit: a case-control study
Arcanjo, A. B. B., & Beccária, L. M. (2023) · Revista Latino-Americana de Enfermagem · doi:10.1590/1518-8345.6224.3864 · Cited by 12 · see citing works
“Extubation is considered when the endolaryngeal prosthesis is removed without the need for reintubation within the next 48 hours or within seven days(15).”
BackgroundInfluentialHenzel, M. K., Shultz, J. M., Dyson‐Hudson, T. A., Svircev, J. N., DiMarco, A. F., & Gater, D. R. (2020) · Journal of the American College of Emergency Physicians Open · doi:10.1002/emp2.12282 · Cited by 12 · see citing works
Racca, F., Finder, J. D., Mercuri, E. M., Vianello, A., Chatwin, M., Amaddeo, A., Crescimanno, G., Trucco, F., Sheehan, D. W., Barberis, L., et al. (2025) · Pediatric Pulmonology · doi:10.1002/ppul.71113 · Cited by 11 · see citing works
Self-citationUser‐perceived impact of long‐term mechanical assisted cough in paediatric neurodisability
Hov, B., Andersen, T. M., Toussaint, M., Mikalsen, I. B., Vollsæter, M., Markussen, H., Indrekvam, S., & Hovland, V. (2023) · Developmental Medicine & Child Neurology · doi:10.1111/dmcn.15543 · Cited by 11 · see citing works
“In NMDs, airway secretion retention is mainly due to respiratory muscle weakness and MIE treatment is thus recommended.(2,6) In disorders originating from the CNS, excessive airway secretion may be more complex, with abnormal laryngeal and skeletal muscle tone, kyphoscoliosis, aspiration, dysphagia, and decreased coug…”
BackgroundInfluentialSelf-citationPredictors of Peak Expiratory Cough Flow in Individuals with Amyotrophic Lateral Sclerosis
Gray, L. T., McElheny, K. L., Vasilopoulos, T., Wymer, J. P., Smith, B. K., & Plowman, E. K. (2022) · Dysphagia · doi:10.1007/s00455-022-10503-8 · Cited by 10 · see citing works
“Specifically, upper airway collapse, turbulence of the pharyngeal tissue, and difficulty coordinating respiratory movements lead to inaccurate flow and pressure readings [6, 29].”
BackgroundAirway Clearance Strategies and Secretion Management in Amyotrophic Lateral Sclerosis
McHenry, K. L. (2023) · Respiratory Care · doi:10.4187/respcare.11215 · Cited by 10 · see citing works
“45 Advantages of this approach in ALS are that coordination with the procedures and limitations associated with bulbar dysfunction are avoided.”
Usefulness of Oscillations Added to Mechanical In-Exsufflation in Amyotrophic Lateral Sclerosis
Sancho, J., Burés, E., Ferrer, S., Bondía, E., & Servera, E. (2019) · Respiratory Care · doi:10.4187/respcare.07202 · Cited by 10 · see citing works
Self-citationYorimoto, K., Ariake, Y., Saotome, T., Mori‐Yoshimura, M., Tsukamoto, T., Takahashi, Y., & Kobayashi, Y. (2020) · Progress in Rehabilitation Medicine · doi:10.2490/prm.20200011 · Cited by 10 · see citing works
Dale, C., Mckim, D. A., Amin, R., Carbone, S., Fisher, T., Goldstein, R. S., Katz, S. L., Gershon, A. S., Leasa, D. J., Nonoyama, M. L., et al. (2020) · Respiratory Care · doi:10.4187/respcare.07534 · Cited by 10 · see citing works
“MI-E therapy is a combination of invasive (ie, advanced airway) and noninvasive (ie, face mask) methods that clears respiratory secretions by applying positive pressure, followed by a rapid shift to negative pressure, thereby simulating a cough.(10,11) Early and appropriate use of MI-E with noninvasive ventilation ena…”
MethodLachal, R., Louis, B., Subtil, F., & Guérin, C. (2019) · Respiratory Care · doi:10.4187/respcare.06478 · Cited by 10 · see citing works
Chronic Neuromuscular Respiratory Failure and Home Assisted Ventilation
Carmona, H. D., Graustein, A. D., & Benditt, J. O. (2023) · Annual Review of Medicine · doi:10.1146/annurev-med-043021-013620 · Cited by 9 · see citing works
Noninvasive respiratory assistance as aid for respiratory care in neuromuscular disorders
Graustein, A. D., Carmona, H. D., & Benditt, J. O. (2023) · Frontiers in Rehabilitation Sciences · doi:10.3389/fresc.2023.1152043 · Cited by 9 · see citing works
Corti, S. P., Sansone, V., Bitetti, I., Brolatti, N., Gadaleta, G., Patanella, A. K., Coratti, G., & Mercuri, E. M. (2025) · Neuromuscular Disorders · doi:10.1016/j.nmd.2025.105278 · Cited by 9 · see citing works
Kulnik, S. T. (2018) · Medical Hypotheses · doi:10.1016/j.mehy.2018.08.004 · Cited by 9 · see citing works
“A sub-group of 20 patients with weak volitional cough (mean PCF 220 L/min, SD 80) showed higher PCF during capsaicin-induced reflex cough than in maximal volitional cough (table 1).”
BackgroundInfluentialHealth Care Use, Costs, and Survival Trajectory of Home Mechanical Insufflation-Exsufflation
Rose, L., Fisher, T., Pizzuti, R., Amin, R., Croxford, R., Dale, C., Goldstein, R. S., Katz, S. L., Leasa, D. J., Mckim, D. A., et al. (2021) · Respiratory Care · doi:10.4187/respcare.09263 · Cited by 9 · see citing works
“%) were hospitalized in the follow-up period (mean SD 7.5 [5.8] months).”
InfluentialLa kinésithérapie respiratoire en pédiatrie
Audag, N., Dubus, J. ‐., & Combret, Y. (2022) · Revue des Maladies Respiratoires · doi:10.1016/j.rmr.2022.05.001 · Cited by 9 · see citing works
Effects of Air Stacking on Dyspnea and Lung Function in Neuromuscular Diseases
Pellegrino, G. M., Corbo, M., Marco, F. D., Pompilio, P. P., Dellacà, R. L., Banfi, P. I., Pellegrino, R., & Papa, G. F. S. (2021) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/j.apmr.2021.01.092 · Cited by 9 · see citing works
Airway Clearance in Neuromuscular Disease
Sheers, N. L., Andersen, T. M., & Chatwin, M. (2024) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2024.04.009 · Cited by 8 · see citing works
Self-citationSteindor, M., Pichler, A., Heitschmidt, L., Pitsikoulis, E., Kavvalou, A., Orhan, E., Olivier, M., & Stehling, F. (2022) · BMC Pulmonary Medicine · doi:10.1186/s12890-022-02012-z · Cited by 8 · see citing works
Upper Airway and Translaryngeal Resistance During Mechanical Insufflation-Exsufflation
Andersen, T. M., Brekka, A. K., Fretheim‐Kelly, Z. L., Luján, M., Heimdal, J., Clemm, H. H., Halvorsen, T., Fondenes, O., Nilsen, R. M., Røksund, O. D., et al. (2024) · CHEST Journal · doi:10.1016/j.chest.2024.08.022 · Cited by 8 · see citing works
Self-citationDiagnosis and Care of Infants and Children with Pompe Disease
Hahn, A., Hennermann, J. B., Huemer, M., Kampmann, C., Marquardt, T., Mengel, E., Müller‐Felber, W., Muschol, N., Rohrbach, M., & Stehling, F. (2020) · Klinische Pädiatrie · doi:10.1055/a-1110-7335 · Cited by 8 · see citing works
“Cough insufficiency can be as - sessed by measuring the peak cough flow [32] and is treated by ap - plication of an airway clearance technique in addition to conven - tional physiotherapy [7].”
Afenigus, A. D., Mulugeta, H., Bewket, B., Ayenew, T., Getnet, A., Akalu, T. Y., Alamneh, Y. M., & Tsehay, B. (2021) · International Journal of Africa Nursing Sciences · doi:10.1016/j.ijans.2021.100299 · Cited by 8 · see citing works
Objective measurement of lung volume recruitment therapy: laboratory and clinical validation
Naughton, P., Sheers, N. L., Berlowitz, D. J., Howard, M. E., Mckim, D. A., & Katz, S. L. (2021) · BMJ Open Respiratory Research · doi:10.1136/bmjresp-2021-000918 · Cited by 8 · see citing works
Self-citationNarayan, S., Pietrusz, A., Allen, J., DiMarco, M., Docherty, K., Emery, N. C., Ennis, M., Flesher, R., Foo, W., Freebody, J., et al. (2022) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-210707 · Cited by 8 · see citing works
Getting It Right in Restrictive Lung Disease
Carlucci, A., & Poli, B. F. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12103353 · Cited by 7 · see citing works
“Early and appropriate use of cough augmentation techniques, such as mechanical cough assist (a device that clears secretions by applying a positive pressure to the airway then rapidly shifting to a negative pressure) combined with HNIV can improve respiratory function, ensuring fewer complications, reducing emergency…”
Background
- Authors
- Chatwin, M., Toussaint, M., Gonçalves, M. R., Sheers, N., Mellies, U., Gonzales-Bermejo, J., Sancho, J., Fauroux, B., Andersen, T., Hov, B., Nygren-Bonnier, M., Lacombe, M., Pernet, K., Kampelmacher, M., Devaux, C., Kinnett, K., Sheehan, D., Rao, F., Villanova, M., Berlowitz, D., & Morrow, B. M.
- Affiliations
- Royal Brompton & Harefield NHS Foundation Trust (GB)
- Universidade do Porto (PT)
- Institute for Breathing and Sleep (AU)
- University of Duisburg-Essen (DE)
- Hôpital Necker-Enfants Malades (FR)
- Haukeland University Hospital (NO)
- Oslo University Hospital (NO)
- Assistance Publique – Hôpitaux de Paris (FR)
- University Medical Center Utrecht (NL)
- Association Francaise contre les Myopathies (FR)
- Women & Children's Hospital of Buffalo (US)
- University of Milan (IT)
- University of Cape Town (ZA)
- Corresponding author
- Chatwin, Michelle
- ORCID
- Venue
- Respiratory Medicine
- Publisher
- Elsevier BV
- Published
- 2018-03
- Volume
- 136
- Pages
- 98-110
- ISSN
- 0954-6111 (ISSN-L)
- OpenAlex
- W2791843842
- Cited by
- 325
- References
- 127
- Citations by year
- 2026: 31 · 2025: 45 · 2024: 45 · 2023: 58 · 2022: 45 · 2021: 35 · 2020: 29 · 2019: 26 · 2018: 11
- FWCI
- 4.51
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Respiratory Medicine (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Universitätsbibliographie, Universität Duisburg-Essen (submittedVersion)
- Funders
- NIHR Respiratory Disease Biomedical Research Unit at the Royal Brompton and Harefield NHS Foundation Trust and Imperial College London
- “Investissement d’Avenir” ANR-10-AIHU 06 of the French Government
- ResMed via the Royal Brompton Hospital
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cystic Fibrosis Research Advances
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Respiratory and Cough-Related Research
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Respiratory Support and Mechanisms
- Keywords
- airway clearance techniques, neuromuscular disorders, cough augmentation, secretion mobilization, infants and children, evidence base
- MeSH terms
- Inhalation, Cough, Humans, Lung Volume Measurements, Mucociliary Clearance, Neuromuscular Diseases, Respiration, Artificial, Respiratory Insufficiency, Respiratory Muscles
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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