Multimodal physiological correlates of dyspnea ratings during breath-holding in healthy humans.

Air hunger Apnea Breath-holding Breathing drive Dyspnea

Journal

European journal of applied physiology
ISSN: 1439-6327
Titre abrégé: Eur J Appl Physiol
Pays: Germany
ID NLM: 100954790

Informations de publication

Date de publication:
10 Oct 2024
Historique:
received: 25 03 2024
accepted: 25 09 2024
medline: 11 10 2024
pubmed: 11 10 2024
entrez: 10 10 2024
Statut: aheadofprint

Résumé

Dyspnea is associated with fear and intense suffering and is often assessed using visual analog scales (VAS) or numerical rating scales (NRS). However, the physiological correlates of such ratings are not well known. Using the voluntary breath-holding model of induced dyspnea, we studied healthy volunteers to investigate the temporal relationship between dyspnea, the neural drive to breathe assessed in terms of involuntary thoracoabdominal movements (ITMs) and neurovegetative responses. Twenty-three participants (10 men; median [interquartile range] age 21 [20-21]) performed three consecutive breath-holds with the continuous assessment of dyspnea (urge-to-breathe) using a 10 cm VAS, thoracic and abdominal circumferences measured with piezoelectric belt-mounted transducers, heart rate and heart rate variability (HRV), and galvanic skin response (GSR). Urge-to-breathe VAS at the onset of ITMs (gasping point) was identified visually or algorithmically. Urge-to-breathe VAS at the end of the breath-hold was 9.7 [8.6-10] cm. Total breath-hold duration was 93 [69-130] s. Urge-to-breathe VAS, ITM, heart rate, HRV, and GSR significantly increased during breath-hold. Urge-to-breathe VAS correlated with the magnitude of the thoracic and abdominal movements (rho = 0.51 and rho = 0.59, respectively, p < 0.001). The urge-to-breathe ratings corresponding with ITM onset were 3.0 [2.0-4.7] cm and 3.0 [1.0-4.0] cm for visual and algorithmic detection, respectively (p = 0.782). An urge-to-breathe VAS of 3 cm (30% of full scale on a 10 cm VAS) corresponds to a physiological turning point during the physiological response to voluntary breath-holding in healthy humans.

Identifiants

pubmed: 39387934
doi: 10.1007/s00421-024-05627-8
pii: 10.1007/s00421-024-05627-8
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : La Fondation pour la Recherche Médicale
ID : FDM201906008876

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Bakdash JZ, Marusich LR (2017) Repeated measures correlation. Front Psychol 8:456. https://doi.org/10.3389/fpsyg.2017.00456
doi: 10.3389/fpsyg.2017.00456 pubmed: 28439244 pmcid: 5383908
Banzett RB, Lansing RW, Reid MB et al (1989) “Air hunger” arising from increased PCO2 in mechanically ventilated quadriplegics. Respir Physiol 76:53–67. https://doi.org/10.1016/0034-5687(89)90017-0
doi: 10.1016/0034-5687(89)90017-0 pubmed: 2499025
Banzett RB, Lansing RW, Brown R et al (1990) “Air hunger” from increased PCO2 persists after complete neuromuscular block in humans. Respir Physiol 81:1–17. https://doi.org/10.1016/0034-5687(90)90065-7
doi: 10.1016/0034-5687(90)90065-7 pubmed: 2120757
Banzett RB, Lansing RW, Evans KC, Shea SA (1996) Stimulus-response characteristics of CO
doi: 10.1016/0034-5687(95)00050-X pubmed: 8822220
Banzett RB, Lansing RW, Binks AP (2021) Air hunger: a primal sensation and a primary element of dyspnea. Compr Physiol 11:1449–1483. https://doi.org/10.1002/cphy.c200001
doi: 10.1002/cphy.c200001 pubmed: 33577128 pmcid: 10986303
Başoğlu M (2017) Effective management of breathlessness: a review of potential human rights issues. Eur Respir J 49:1602099. https://doi.org/10.1183/13993003.02099-2016
doi: 10.1183/13993003.02099-2016 pubmed: 28546267
Bureau C, Decavèle M, Campion S et al (2021) Proportional assist ventilation relieves clinically significant dyspnea in critically ill ventilated patients. Ann Intensiv Care 11:177. https://doi.org/10.1186/s13613-021-00958-7
doi: 10.1186/s13613-021-00958-7
Bureau C, Dres M, Morawiec E et al (2022) Dyspnea and the electromyographic activity of inspiratory muscles during weaning from mechanical ventilation. Ann Intensiv Care 12:50. https://doi.org/10.1186/s13613-022-01025-5
doi: 10.1186/s13613-022-01025-5
Campbell ML (2007) Fear and pulmonary stress behaviors to an asphyxial threat across cognitive states. Res Nurs Health 30:572–583. https://doi.org/10.1002/nur.20212
doi: 10.1002/nur.20212 pubmed: 18022811
Dangers L, Montlahuc C, Kouatchet A et al (2018) Dyspnoea in patients receiving noninvasive ventilation for acute respiratory failure: prevalence, risk factors and prognostic impact: a prospective observational study. Eur Respir J 52:1702637. https://doi.org/10.1183/13993003.02637-2017
doi: 10.1183/13993003.02637-2017 pubmed: 29976650
Decavèle M, Rivals I, Persichini R et al (2022) Prognostic value of the intensive care respiratory distress observation scale on ICU admission. Respir Care 67:823–832. https://doi.org/10.4187/respcare.09601
doi: 10.4187/respcare.09601 pubmed: 35440498
Decavèle M, Bureau C, Campion S et al (2023) Interventions relieving dyspnea in intubated patients show responsiveness of the mechanical ventilation-respiratory distress observation scale. Am J Respir Crit Care Med 208:39–48. https://doi.org/10.1164/rccm.202301-0188OC
doi: 10.1164/rccm.202301-0188OC pubmed: 36973007
Demoule A, Similowski T (2019) Respiratory suffering in the ICU: time for our next great cause. Am J Respir Crit Care Med 199:1302–1304. https://doi.org/10.1164/rccm.201812-2248ED
doi: 10.1164/rccm.201812-2248ED pubmed: 30562045 pmcid: 6543714
Demoule A, Hajage D, Messika J et al (2022) Prevalence, intensity and clinical impact of dyspnea in critically ill patients receiving invasive ventilation. Am J Respir Crit Care Med 205(8):917–926
doi: 10.1164/rccm.202108-1857OC pubmed: 35061577
Demoule A, Baptiste A, Thille AW et al (2024a) Dyspnea is severe and associated with a higher intubation rate in de novo acute hypoxemic respiratory failure. Crit Care Lond Engl 28:174. https://doi.org/10.1186/s13054-024-04903-5
doi: 10.1186/s13054-024-04903-5
Demoule A, Decavele M, Antonelli M et al (2024b) Dyspnoea in acutely ill mechanically ventilated adult patients: an ERS/ESICM statement. Intensiv Care Med 50:159–180. https://doi.org/10.1007/s00134-023-07246-x
doi: 10.1007/s00134-023-07246-x
Demoule A, Decavele M, Antonelli M et al (2024c) Dyspnoea in acutely ill mechanically ventilated adult patients: an ERS/ESICM statement. Eur Respir J 63:2300347. https://doi.org/10.1183/13993003.00347-2023
doi: 10.1183/13993003.00347-2023 pubmed: 38387998
Evans KC, Banzett RB, Adams L et al (2002) BOLD fMRI identifies limbic, paralimbic, and cerebellar activation during air hunger. J Neurophysiol 88:1500–1511. https://doi.org/10.1152/jn.2002.88.3.1500
doi: 10.1152/jn.2002.88.3.1500 pubmed: 12205170
Haugdahl HS, Storli SL, Meland B et al (2015) Underestimation of patient breathlessness by nurses and physicians during a spontaneous breathing trial. Am J Respir Crit Care Med 192:1440–1448. https://doi.org/10.1164/rccm.201503-0419OC
doi: 10.1164/rccm.201503-0419OC pubmed: 26669474
Kochovska S, Ferreira D, Chang S et al (2024) Disability and long-term breathlessness: a cross-sectional, population study. BMJ Open Respir Res 11:e002029. https://doi.org/10.1136/bmjresp-2023-002029
doi: 10.1136/bmjresp-2023-002029 pubmed: 39038915 pmcid: 11268077
Kuroda T, Masaoka Y, Kasai H et al (2012) Sharing breathlessness: investigating respiratory change during observation of breath-holding in another. Respir Physiol Neurobiol 180:218–222. https://doi.org/10.1016/j.resp.2011.11.010
doi: 10.1016/j.resp.2011.11.010 pubmed: 22146376
Le Marec J, Hajage D, Decavèle M et al (2024) High airway occlusion pressure is associated with dyspnea and increased mortality in critically Ill mechanically ventilated patients. Am J Respir Crit Care Med 210:201–210. https://doi.org/10.1164/rccm.202308-1358OC
doi: 10.1164/rccm.202308-1358OC pubmed: 38319128
Lin YC, Lally DA, Moore TO, Hong SK (1974) Physiological and conventional breath-hold breaking points. J Appl Physiol 37:291–296. https://doi.org/10.1152/jappl.1974.37.3.291
doi: 10.1152/jappl.1974.37.3.291 pubmed: 4415069
McKay LC, Adams L, Frackowiak RSJ, Corfield DR (2008) A bilateral cortico-bulbar network associated with breath holding in humans, determined by functional magnetic resonance imaging. Neuroimage 40:1824–1832. https://doi.org/10.1016/j.neuroimage.2008.01.058
doi: 10.1016/j.neuroimage.2008.01.058 pubmed: 18343687
Morélot-Panzini C, Gilet H, Aguilaniu B et al (2016) Real-life assessment of the multidimensional nature of dyspnoea in COPD outpatients. Eur Respir J 47:1668–1679. https://doi.org/10.1183/13993003.01998-2015
doi: 10.1183/13993003.01998-2015 pubmed: 27076585
Morélot-Panzini C, Perez T, Sedkaoui K et al (2018) The multidimensional nature of dyspnoea in amyotrophic lateral sclerosis patients with chronic respiratory failure: air hunger, anxiety and fear. Respir Med 145:1–7. https://doi.org/10.1016/j.rmed.2018.10.010
doi: 10.1016/j.rmed.2018.10.010 pubmed: 30509697
Nicholas CL, Bei B, Worsnop C et al (2010) Motor unit recruitment in human genioglossus muscle in response to hypercapnia. Sleep 33:1529–1538
doi: 10.1093/sleep/33.5.1529 pubmed: 21102995 pmcid: 2954703
Niérat M-C, Laviolette L, Hudson A et al (2017) Experimental dyspnea as a stressor: differential cardiovegetative responses to inspiratory threshold loading in healthy men and women. J Appl Physiol Bethesda Md 123:205–212. https://doi.org/10.1152/japplphysiol.00078.2017
doi: 10.1152/japplphysiol.00078.2017
Nishino T (2009) Pathophysiology of dyspnea evaluated by breath-holding test: studies of furosemide treatment. Respir Physiol Neurobiol 167:20–25. https://doi.org/10.1016/j.resp.2008.11.007
doi: 10.1016/j.resp.2008.11.007 pubmed: 19070689
Parshall MB, Schwartzstein RM, Adams L et al (2012) An official American thoracic society statement: update on the mechanisms, assessment, and management of dyspnea. Am J Respir Crit Care Med 185:435–452. https://doi.org/10.1164/rccm.201111-2042ST
doi: 10.1164/rccm.201111-2042ST pubmed: 22336677 pmcid: 5448624
Pierre D (1965) Hazard of hypoxia during diving. In: Rahn H, Yokoyama T (eds) Physiology of breath-hold diving and the ama of Japan. National Academy of Science National Research Council
Raji RK, Miao X, Wan A et al (2019) Knitted piezoresistive smart chest band and its application for respiration patterns assessment. J Eng Fibers Fabr 14:1558925019868474. https://doi.org/10.1177/1558925019868474
doi: 10.1177/1558925019868474
Ries AL (2006) Impact of chronic obstructive pulmonary disease on quality of life: the role of dyspnea. Am J Med 119:12–20. https://doi.org/10.1016/j.amjmed.2006.08.003
doi: 10.1016/j.amjmed.2006.08.003 pubmed: 16996895
Schmidt M, Kindler F, Gottfried SB et al (2013) Dyspnea and surface inspiratory electromyograms in mechanically ventilated patients. Intensiv Care Med 39:1368–1376. https://doi.org/10.1007/s00134-013-2910-3
doi: 10.1007/s00134-013-2910-3
Stevens JP, Dechen T, Schwartzstein R et al (2018) Prevalence of dyspnea among hospitalized patients at the time of admission. J Pain Symptom Manage 56:15-22.e2. https://doi.org/10.1016/j.jpainsymman.2018.02.013
doi: 10.1016/j.jpainsymman.2018.02.013 pubmed: 29476798 pmcid: 6317868
Stevens JP, Sheridan AR, Bernstein HB et al (2019) A multidimensional profile of dyspnea in hospitalized patients. Chest 156:507–517. https://doi.org/10.1016/j.chest.2019.04.128
doi: 10.1016/j.chest.2019.04.128 pubmed: 31128117 pmcid: 7090324
Stevens JP, Dechen T, Schwartzstein RM et al (2021) Association of dyspnoea, mortality and resource use in hospitalised patients. Eur Respir J 58:1902107. https://doi.org/10.1183/13993003.02107-2019
doi: 10.1183/13993003.02107-2019 pubmed: 33653806
Topulos GP, Lansing RW, Banzett RB (1993) The experience of complete neuromuscular blockade in awake humans. J Clin Anesth 5:369–374. https://doi.org/10.1016/0952-8180(93)90099-z
doi: 10.1016/0952-8180(93)90099-z pubmed: 8105828
Vigran HJ, Kapral AG, Tytell ED, Kao MH (2019) Manipulating the perception of time affects voluntary breath-holding duration. Physiol Rep 7(23):e14309
doi: 10.14814/phy2.14309 pubmed: 31833235 pmcid: 6908740
Whitelaw WA, McBride B, Amar J, Corbet K (1981) Respiratory neuromuscular output during breath holding. J Appl Physiol 50:435–443. https://doi.org/10.1152/jappl.1981.50.2.435
doi: 10.1152/jappl.1981.50.2.435 pubmed: 6451605

Auteurs

Maxens Decavèle (M)

APHP Sorbonne Université, INSERM, UMRS1158 Neurophysiologie Respiratoire Expérimentale Et Clinique, 47-83 Boulevard de L'Hôpital, 75013, Paris, France.
Service de Médecine Intensive Et Réanimation (Département R3S), Groupe Hospitalier Universitaire APHP-Sorbonne Université, Site Pitié-Salpêtrière, 75013, Paris, France.

Marie-Cécile Nierat (MC)

APHP Sorbonne Université, INSERM, UMRS1158 Neurophysiologie Respiratoire Expérimentale Et Clinique, 47-83 Boulevard de L'Hôpital, 75013, Paris, France.

Louis Laviolette (L)

Faculté de Médecine, Université Laval, Québec, Canada.
Centre de Recherche de L'Institut Universitaire de Cardiologie Et de Pneumologie de Québec (CRIUCPQ), Québec, Canada.

Nicolas Wattiez (N)

APHP Sorbonne Université, INSERM, UMRS1158 Neurophysiologie Respiratoire Expérimentale Et Clinique, 47-83 Boulevard de L'Hôpital, 75013, Paris, France.

Damien Bachasson (D)

APHP Sorbonne Université, INSERM, UMRS1158 Neurophysiologie Respiratoire Expérimentale Et Clinique, 47-83 Boulevard de L'Hôpital, 75013, Paris, France.

Gabriel Kemoun (G)

APHP Sorbonne Université, INSERM, UMRS1158 Neurophysiologie Respiratoire Expérimentale Et Clinique, 47-83 Boulevard de L'Hôpital, 75013, Paris, France. gabriel.kemoun@gmail.com.

Capucine Morélot-Panzini (C)

APHP Sorbonne Université, INSERM, UMRS1158 Neurophysiologie Respiratoire Expérimentale Et Clinique, 47-83 Boulevard de L'Hôpital, 75013, Paris, France.
Service de Pneumologie (Département R3S), Groupe Hospitalier Universitaire APHP-Sorbonne Université, Site Pitié-Salpêtrière, 75013, Paris, France.

Alexandre Demoule (A)

APHP Sorbonne Université, INSERM, UMRS1158 Neurophysiologie Respiratoire Expérimentale Et Clinique, 47-83 Boulevard de L'Hôpital, 75013, Paris, France.
Service de Médecine Intensive Et Réanimation (Département R3S), Groupe Hospitalier Universitaire APHP-Sorbonne Université, Site Pitié-Salpêtrière, 75013, Paris, France.

Thomas Similowski (T)

APHP Sorbonne Université, INSERM, UMRS1158 Neurophysiologie Respiratoire Expérimentale Et Clinique, 47-83 Boulevard de L'Hôpital, 75013, Paris, France.
Département R3S, Groupe Hospitalier Universitaire APHP-Sorbonne Université, Site Pitié-Salpêtrière, 75013, Paris, France.

Classifications MeSH