Mucus Transpiration as the Basis for Chronic Cough and Cough Hypersensitivity.

Bronchoconstriction Cough Cough hypersensitivity Dehydration Hypertonic aerosols Mucus Transpiration

Journal

Lung

ISSN: 1432-1750

Titre abrégé: Lung

Pays: United States

ID NLM: 7701875

Informations de publication

Date de publication:
22 Dec 2023

Historique:

received: 04 10 2023

accepted: 22 11 2023

medline: 23 12 2023

pubmed: 23 12 2023

entrez: 22 12 2023

Statut: aheadofprint

Résumé

Chronic cough is characterized by a state of cough hypersensitivity. We analyze the process of transpiration, by which water appears to evaporate from laryngeal and tracheal mucus as from the surface of a leaf, as a potential cause of cough hypersensitivity. In this process, osmotic pressure differences form across mucus, pulling water toward the air, and preventing mucus dehydration. Recent research suggests that these osmotic differences grow on encounter with dry and dirty air, amplifying pressure on upper airway epithelia and initiating a cascade of biophysical events that potentially elevate levels of ATP, promote inflammation and acidity, threaten water condensation, and diminish mucus water permeability. Among consequences of this inflammatory cascade is tendency to cough. Studies of isotonic, hypotonic, and hypertonic aerosols targeted to the upper airways give insights to the nature of mucus transpiration and its relationship to a water layer that forms by condensation in the upper airways on exhalation. They also suggest that, while hypertonic NaCl and mannitol may provoke cough and bronchoconstriction, hypertonic salts with permeating anions and non-permeating cations may relieve these same upper respiratory dysfunctions. Understanding of mucus transpiration and its role in cough hypersensitivity can lead to new treatment modalities for chronic cough and other airway dysfunctions promoted by the breathing of dry and dirty air.

Identifiants

DOI: 10.1007/s00408-023-00664-0 PMID: 38135857

pubmed: 38135857

doi: 10.1007/s00408-023-00664-0

pii: 10.1007/s00408-023-00664-0

doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

Informations de copyright

Références

Chung KF, McGarvey L, Song WJ, Chang AB, Lai K, Canning BJ et al (2022) Cough hypersensitivity and chronic cough. Nat Rev Dis Primers 8(1):45

pubmed: 35773287 pmcid: 9244241 doi: 10.1038/s41572-022-00370-w

Chung KF, McGarvey L, Mazzone SB (2013) Chronic cough as a neuropathic disorder. Lancet Respir Med. 1(5):414–422

pubmed: 24429206 doi: 10.1016/S2213-2600(13)70043-2

Edwards DA, Chung KF (2023) Breathing dry air promotes inflammation, activates neural pathways and disrupts clearance by osmotic stresses imparted on airway epithelia. Q Rev Biophys Discov 4:e3

Purokivi M, Koskela H, Brannan JD, Kontra K (2011) Cough response to isocapnic hyperpnoea of dry air and hypertonic saline are interrelated. Cough 7(1):8

pubmed: 21999754 pmcid: 3205007 doi: 10.1186/1745-9974-7-8

Eklund LM, Sköndal Å, Tufvesson E, Sjöström R, Söderström L, Hanstock HG, Sandström T, Stenfors N (2022) Cold air exposure at - 15 °C induces more airway symptoms and epithelial stress during heavy exercise than rest without aggravated airway constriction. Eur J Appl Physiol 122(12):2533–2544

pubmed: 36053365 pmcid: 9613713 doi: 10.1007/s00421-022-05004-3

Musseau D (2016) Mouth breathing and some of its consequences. Int J Orthod Milwaukee 27(2):51–54

pubmed: 29799704

Simpson AJ, Romer LM, Kippelen P (2017) Exercise-induced dehydration alters pulmonary function but does not modify airway responsiveness to dry air in athletes with mild asthma. J Appl Physiol 122(5):1329–1335

pubmed: 28280109 pmcid: 5451531 doi: 10.1152/japplphysiol.01114.2016

Wei W, Sun Z, He S, Zhang W, Chen S, Cao YN, Wang N (2022) Mechanical ventilation induces lung and brain injury through ATP production, P2Y1 receptor activation and dopamine release. Bioeng 13(2):2346–2359

Zhang M, Sykes DL, Sadofsky LR, Morice AH (2022) ATP, an attractive target for the treatment of refractory chronic cough. Purinergic Signal 18(3):289–305

pubmed: 35727480 pmcid: 9209634 doi: 10.1007/s11302-022-09877-z

Romaszko-Wojtowicz A, Cymes I, Dragańska E, Doboszyńska A, Romaszko J, Glińska-Lewczuk K (2020) Relationship between biometeorological factors and the number of hospitalizations due to asthma. Sci Rep 10(1):9593

pubmed: 32533079 pmcid: 7293260 doi: 10.1038/s41598-020-66746-8

D’Amato M, Molino A, Calabrese G, Cecchi L, Annesi-Maesano I, D’Amato G (2018) The impact of cold on the respiratory tract and its consequences to respiratory health. Clin Transl Allergy. https://doi.org/10.1186/213601-018-0208-9

doi: 10.1186/213601-018-0208-9 pubmed: 29997887 pmcid: 6031196

Kudo E, Song E, Yockey LJ, Rakib T, Wong PW, Homer RJ, Iwasaki A (2019) Influenza worsens dry air Low ambient humidity impairs barrier function and innate resistance against influenza infection. Proc of the Natl Acad of Sci 116(22):10905–10910

doi: 10.1073/pnas.1902840116

Mecenas P, Bastos R, Vallinoto A, Normando D (2020) Effects of temperature and humidity on the spread of COVID-19: A systematic review. PLoS ONE 15(9):e0238339

pubmed: 32946453 pmcid: 7500589 doi: 10.1371/journal.pone.0238339

Kelly SJ, Martinsen P, Tatkov S (2021) Rapid changes in mucociliary transport in the tracheal epithelium caused by unconditioned room air or nebulized hypertonic saline and mannitol are not determined by frequency of beating cilia. Intensive Care Med Exp 9(1):8

pubmed: 33728866 pmcid: 7966670 doi: 10.1186/s40635-021-00374-y

Xing YF, Xu YH, Shi MH, Lian YX (2016) The impact of PM2.5 on the human respiratory system. J Thorac Dis 1:E69–E74

Bolger C, Tufvesson E, Anderson SD, Devereux G, Ayres JG, Bjermer L, Sue-Chu M, Kippelen P (2011) Effect of inspired air conditions on exercise-induced bronchoconstriction and urinary CC16 levels in athletes. J Appl Physiol 111(4):1059–1065

pubmed: 21799131 doi: 10.1152/japplphysiol.00113.2011

Lappharat S, Taneepanichskul N, Reutrakul S, Chirakalwasan N (2018) Effects of bedroom environmental conditions on the severity of obstructive sleep apnea. J Clin Sleep Med 14(4):565–573

pubmed: 29609708 pmcid: 5886434 doi: 10.5664/jcsm.7046

Tatsuya U, Yoshikawa T, Ueda YK, Orita K, Fujimoto S (2011) Effects of acute prolonged strenuous exercise on the salivary stress markers and inflammatory cytokines. Jpn J Phys Fitness Sports Med 60(3):295–304

doi: 10.7600/jspfsm.60.295

Boulet LP, Turmel J (2019) Cough in exercise and athletes. Pulm Pharmacol Ther 55:67–74

pubmed: 30771475 doi: 10.1016/j.pupt.2019.02.003

Vanderlei FM, Moreno IL, Vanderlei LC, Pastre CM, de Abreu LC, Ferreira C (2013) Effects of different protocols of hydration on cardiorespiratory parameters during exercise and recovery. Int Arch Med 6(1):33

pubmed: 23968198 pmcid: 3765387 doi: 10.1186/1755-7682-6-33

McFadden ER Jr, Pichurko BM, Bowman HF, Ingenito E, Burns S, Dowling N, Solway J (1985) Thermal mapping of the airways in humans. J Appl Physiol 58(2):564–570

pubmed: 3980358 doi: 10.1152/jappl.1985.58.2.564

Strauss RH, McFadden ER Jr, Ingram RH Jr, Deal EC Jr, Jaeger JJ (1978) Influence of heat and humidity on the airway obstruction induced by exercise in asthma. J Clin Invest 61(2):433–440

pubmed: 621282 pmcid: 372554 doi: 10.1172/JCI108954

Haut B, Karamaoun C, Mauroy B, Sobac B (2023) Water and heat exchanges in mammalian lungs. Sci Rep 13(1):6636

pubmed: 37095142 pmcid: 10126058 doi: 10.1038/s41598-023-33052-y

Haut B, Nonclercq A, Buess A, Rabineau J, Rigaut C, Sobac B (2021) Comprehensive analysis of heat and water exchanges in the human lungs. Front Physiol 8(12):649497

doi: 10.3389/fphys.2021.649497

Lin CL, Tawhai MH, McLennan G, Hoffman EA (2007) Characteristics of the turbulent laryngeal jet and its effect on airflow in the human intra-thoracic airways. Respir Physiol Neurobiol 157(2–3):295–309

pubmed: 17360247 pmcid: 2041885 doi: 10.1016/j.resp.2007.02.006

Wheeler T, Stroock A (2008) The transpiration of water at negative pressures in a synthetic tree. Nature 455:208–212

pubmed: 18784721 doi: 10.1038/nature07226

Burkhardt J, Hunsche M (2013) “Breath figures” on leaf surfaces-formation and effects of microscopic leaf wetness. Front Plant Sci 24(4):422

Van Hove LWA, Adema EH (1996) The effective thickness of water films on leaves. Atmos Environ 30(16):2933–2936

doi: 10.1016/1352-2310(96)00012-X

Reeves ER, Molloy K, McElvaney NG et al (2012) Hypertonic saline in treatment of pulmonary disease in cystic fibrosis. The Scientific World J 2012(465230):11

Vermeulen R, van der Linde J, Abdoola S, van Lierde K, Graham MA (2021) The effect of superficial hydration, with or without systemic hydration, on voice quality in future female professional singers. J Voice 35(5):728–738

pubmed: 32046884 doi: 10.1016/j.jvoice.2020.01.008

Elkins MR, Bye PT (2011) Mechanisms and applications of hypertonic saline. J R Soc Med. 104(Suppl 1):S2–S5

pubmed: 21719889 pmcid: 3128163 doi: 10.1258/JRSM.2011.S11101

George CE, Scheuch G, Seifart U, Inbaraj LR, Chandrasingh S, Nair IK, Hickey AJ, Barer MR, Fletcher E, Field RD, Salzman J, Moelis N, Ausiello D, Edwards DA (2022) COVID-19 symptoms are reduced by targeted hydration of the nose, larynx and trachea. Sci Rep 12(1):4599

pubmed: 35351914 pmcid: 8964810 doi: 10.1038/s41598-022-08609-y

Darwin F (1914) On a method of studying transpiration. Proc Roy Soc Lond 87(595):269–280

Peppin SSL, Elliot JAW, Worster MG (2005) Pressure and relative motion in colloidal suspensions. Phys Fluids 17:053301

doi: 10.1063/1.1915027

von Caemmerer S, Baker N (2007) The biology of transpiration. From guard cells to globe. Plant Physiol. 143(1):3

doi: 10.1104/pp.104.900213

Geng H, Xu Q, Wu M et al (2019) Plant leaves inspired sunlight-driven purifier for high-efficiency clean water production. Nat Commun 10:1512

pubmed: 30944322 pmcid: 6447597 doi: 10.1038/s41467-019-09535-w

Choi YH, Lee SS, Chung KH (2010) Microfluidic actuation and sampling by dehydration of hydrogel. BioChip J 4(1):63–69

doi: 10.1007/s13206-010-4110-3

Lee SJ, Kim H, Ahn S (2015) Water transport in porous hydrogel structures analogous to leaf mesophyll cells. Microfluid Nanofluid 18(5):775–784

doi: 10.1007/s10404-014-1418-7

Martin DK (1995) Water transport in dehydrating hydrogel contact lenses: implications for corneal desiccation. J Biomed Mater Res 29(7):857–865

pubmed: 7593025 doi: 10.1002/jbm.820290711

Etzold MA, Linden PF, Grae Worster M (2021) Transpiration through hydrogels. Journal of Fluid Mechanics 925:A8

doi: 10.1017/jfm.2021.608

Zieliński J, Przybylski J (2012) Ile wody tracimy z oddechem? [How much water is lost during breathing?]. Pneumonol Alergol Pol 80(4):339–342

pubmed: 22714078

Button B, Okada SF, Frederick CB, Thelin WR, Boucher RC (2013) Mechanosensitive ATP release maintains proper mucus hydration of airways. Sci Signal. 6(279):ra46

pubmed: 23757023 pmcid: 3791865 doi: 10.1126/scisignal.2003755

Fowles HE, Rowland T, Wright C, Morice A (2017) Tussive challenge with ATP and AMP: does it reveal cough hypersensitivity? Eur Respir J 49(2):1601452

pubmed: 28179439 doi: 10.1183/13993003.01452-2016

Kanahama T, Tsugawa S, Sato M (2023) Rigidity control mechanism by turgor pressure in plants. Sci Rep 13:2063

pubmed: 36739460 pmcid: 9899264 doi: 10.1038/s41598-023-29294-5

Evans JH, Sanderson MJ (1999) Intracellular calcium oscillations induced by ATP in airway epithelial cells. Am J Physiol 277(1):L30–L41

pubmed: 10409228

Bargon J, Trapnell BC, Chu CS, Rosenthal ER, Yoshimura K, Guggino WB, Dalemans W, Pavirani A, Lecocq JP, Crystal RG (1992) Down-regulation of cystic fibrosis transmembrane conductance regulator gene expression by agents that modulate intracellular divalent cations. Mol Cell Biol 12(4):1872–1878

pubmed: 1372390 pmcid: 369631

Solimando AG, Desantis V, Ribatti D (2022) Mast cells and interleukins. Int J Mol Sci 23(22):14004

pubmed: 36430483 pmcid: 9697830 doi: 10.3390/ijms232214004

Possa SS, Leick EA, Prado CM, Martins MA, Tibério IF (2013) Eosinophilic inflammation in allergic asthma. Front Pharmacol 17(4):46

Wen T, Mingler MK, Wahl B, Khorki ME, Pabst O, Zimmermann N, Rothenberg ME (2014) Carbonic anhydrase IV is expressed on IL-5-activated murine eosinophils. J Immunol 192(12):5481–5489

pubmed: 24808371 doi: 10.4049/jimmunol.1302846

Jia Y, Lee LY (2007) Role of TRPV receptors in respiratory diseases. Biochim Biophys Acta 1772(8):915–927

pubmed: 17346945 doi: 10.1016/j.bbadis.2007.01.013

Cerqueira É, Marinho DA, Neiva HP, Lourenço O (2020) Inflammatory effects of high and moderate intensity exercise-a systematic review. Front Physiol 9(10):1550

doi: 10.3389/fphys.2019.01550

Boucher RC (2004) New concepts of the pathogenesis of cystic fibrosis lung disease. Eur Respir J 23(1):146–158

pubmed: 14738247 doi: 10.1183/09031936.03.00057003

Anderson SD, Daviskas E, Brannan JD, Chan HK (2018) Repurposing excipients as active inhalation agents: the mannitol story. Adv Drug Deliv Rev 133:45–56

pubmed: 29626547 doi: 10.1016/j.addr.2018.04.003

Anderson SD, Charlton B, Weiler JM, Nichols S, Spector SL, Pearlman DS, A305 Study Group (2009) Comparison of mannitol and methacholine to predict exercise-induced bronchoconstriction and a clinical diagnosis of asthma. Respir Res 10(1):4

pubmed: 19161635 pmcid: 2644668 doi: 10.1186/1465-9921-10-4

Niimi A, Nguyen LT, Usmani O, Mann B, Chung KF (2004) Reduced pH and chloride levels in exhaled breath condensate of patients with chronic cough. Thorax 59(7):608–612

pubmed: 15223872 pmcid: 1747079 doi: 10.1136/thx.2003.012906

Sadeghi MH, Wright CE, Hart S, Crooks M, Morice AH (2018) Does FeNO predict clinical characteristics in chronic cough? Lung 196(1):59–64

pubmed: 29177539 doi: 10.1007/s00408-017-0074-6

Vyazmin A, Khramtsov D, Pokusaev B, Nekrasov D, Zakharov N (2019) Experimental study of liquid evaporation from a surface of gel mixture. EPJ Web of Conferences 196:00030

doi: 10.1051/epjconf/201919600030

Martonen TB, Zhang Z, Lessmann RC (1993) Fluid dynamics of the human larynx and upper tracheobronchial airways. Aerosol Sci Technol 19(2):133–156

doi: 10.1080/02786829308959627

Liu S, Liu CC, Froyd KD, Schill GP, Murphy DM, Bui TP, Dean-Day JM, Weinzierl B, Dollner M, Diskin GS, Chen G, Gao RS (2021) Sea spray aerosol concentration modulated by sea surface temperature. Proc of the Natl Academy of Sci 118(9):e2020583118

doi: 10.1073/pnas.2020583118

Field R, Moellis N, Salzman J, Bax A, Ausiello D, Woodword S, Wu X, Domici F, Edwards D (2021) Moisture and airborne salt suppress respiratory droplet generation and may reduce COVID-19 incidence and death. Mol Front J 5:1–10

doi: 10.1142/S2529732521400058

Edwards DA, Man JC, Brand P, Katstra JP, Sommerer K, Stone HA, Nardell E, Scheuch G (2004) Inhaling to mitigate exhaled bioaerosols. Proc Natl Acad Sci 101(50):17383–17388

pubmed: 15583121 pmcid: 536048 doi: 10.1073/pnas.0408159101

Morawska L, Milton DK (2020) It is time to address airborne transmission of coronavirus disease 2019 (COVID-19). Clin Infect Dis 71(9):2311–2313

pubmed: 32628269

Courtney JM, Bax A (2021) Hydrating the respiratory tract: An alternative explanation why masks lower severity of COVID-19. Biophys J 120(6):994–1000

pubmed: 33582134 pmcid: 7879047 doi: 10.1016/j.bpj.2021.02.002

Wang F, Liu J, Zeng H (2020) Interactions of particulate matter and pulmonary surfactant: Implications for human health. Adv Colloid Interface Sci 284:102244

pubmed: 32871405 pmcid: 7435289 doi: 10.1016/j.cis.2020.102244

Datta SS, Preska Steinberg A, Ismagilov RF (2016) Polymers in the gut compress the colonic mucus hydrogel. Proc Natl Acad Sci U S A 113(26):7041–7046

pubmed: 27303035 pmcid: 4932961 doi: 10.1073/pnas.1602789113

Anderson SD, Brannan J, Spring J, Spalding N, Rodwell LT, Chan K, Gonda I, Walsh A, Clark AR (1997) A new method for bronchial-provocation testing in asthmatic subjects using a dry powder of mannitol. Am J Respir Crit Care Med 156(3 Pt 1):758–765

pubmed: 9309990 doi: 10.1164/ajrccm.156.3.9701113

Anderson SD (2016) ‘Indirect’ challenges from science to clinical practice. Eur Clin Respir J 22(3):31096

doi: 10.3402/ecrj.v3.31096

Zuim A-F, Edwards A, Ausiello DA, Bhatta D, Edwards DA Hypertonic aerosols hydrate airways longer and reduce acidification risk with non-permeating cation and permeating anion salts. J Aerosols Med Pulm Drug Deliv (in press)

Sandefur CI, Boucher RC, Elston TC (2017) Mathematical model reveals role of nucleotide signaling in airway surface liquid homeostasis and its dysregulation in cystic fibrosis. Proc Natl Acad Sci USA 114(35):E7272–E7281

pubmed: 28808008 pmcid: 5584404 doi: 10.1073/pnas.1617383114