Abstract
Increased negative intrathoracic pressure that occurs during pharyngeal obstruction can increase thoracic fluid volume that may contribute to lower airway narrowing in individuals with obstructive sleep apnea (OSA) and asthma. Our previous study showed that fluid accumulation in the thorax induced by simulated OSA can increase total respiratory resistance. However, the effect of fluid shift on lower airway narrowing has not been investigated. To examine the effect of fluid accumulation in the thorax on the resistance of the lower airway. Non-asthma participants and individuals with (un)controlled asthma were recruited and underwent a single-day experiment. A catheter with six pressure sensors was inserted through the nose to continuously measure pressure at different sites of the airway, while a pneumotachograph was attached to a mouthpiece to record airflow. To simulate obstructive apneas, participants performed 25 Mueller maneuvers (MMs) while lying supine. Using the recordings of pressure sensor and airflow, total respiratory (RT), lower respiratory components (RL), and upper airway (RUA) resistances were calculated before and after MMs. Generalized estimation equation method was used to find the predictors of RL among variables including age, sex, body mass index, and the effect of MMs and asthma. Eighteen participants were included. Performing MMs significantly increased RT (2.23 ± 2.08 cmH2O/L/s, p = 0.003) and RL (1.52 ± 2.00 cmH2O/L/s, p = 0.023) in participants with asthma, while only RL was increased in non-asthma group (1.96 ± 1.73 cmH2O/L/s, p = 0.039). We found the model with age, and the effect of MMs and asthma severity generated the highest correlation (R2 = 0.69, p < 0.001). We provide evidence that fluid accumulation in the thorax caused by excessive intrathoracic pressure increases RL in both non-asthma and asthma groups. The changes in RL were related to age, having asthma and the effect of simulated OSA. This can explain the interrelationship between OSA and asthma.
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References
Peppard, P. E., T. Young, J. H. Barnet, M. Palta, E. W. Hagen, and K. M. Hla. Increased prevalence of sleep-disordered breathing in adults. Am J Epidemiol. 177(9):1006–1014, 2013.
Teodorescu, M., J. H. Barnet, E. W. Hagen, M. Palta, T. B. Young, and P. E. Peppard. Association between asthma and risk of developing obstructive sleep apnea. JAMA. 313(2):156–164, 2015.
Teodorescu, M., O. Broytman, D. Curran-Everett, et al. Obstructive sleep apnea risk, asthma burden, and lower airway inflammation in adults in the severe asthma research program (SARP) II. J. Allergy Clin. Immunol.: Pract. 3(4):566–575, 2015.
Hermus, G., C. Stonebridge, D. Goldfarb, L. Thériault, F. Bounajm. Cost risk analysis for chronic lung disease in Canada, 2012.
Julien, J. Y., J. G. Martin, P. Ernst, et al. Prevalence of obstructive sleep apnea–hypopnea in severe versus moderate asthma. J. Allergy Clin. Immunol. 124(2):371–376, 2009.
Ten Brinke, A., P. J. Sterk, A. Masclee, et al. Risk factors of frequent exacerbations in difficult-to-treat asthma. Eur. Respir. J. 26(5):812–818, 2005.
Teodorescu, M., D. A. Polomis, M. C. Teodorescu, et al. Association of obstructive sleep apnea risk or diagnosis with daytime asthma in adults. J. Asthma. 49(6):620–628, 2012.
Teodorescu, M., D. A. Polomis, R. E. Gangnon, et al. Asthma control and its relationship with obstructive sleep apnea (OSA) in older adults. Sleep Disord. 2013:1–11, 2013.
Davies, S. E., A. Bishopp, S. Wharton, A. M. Turner, and A. H. Mansur. Does continuous positive airway pressure (CPAP) treatment of obstructive sleep apnoea (OSA) improve asthma-related clinical outcomes in patients with co-existing conditions?-A systematic review. Respir Med. 143:18–30, 2018.
Kauppi, P., P. Bachour, P. Maasilta, and A. Bachour. Long-term CPAP treatment improves asthma control in patients with asthma and obstructive sleep apnoea. Sleep Breath. 20:1217–1224, 2016.
Ioachimescu, O. C., and M. Teodorescu. Integrating the overlap of obstructive lung disease and obstructive sleep apnoea: OLDOSA syndrome. Respirology. 18(3):421–431, 2013.
Bhatawadekar, S. A., M. D. Inman, J. J. Fredberg, et al. Contribution of rostral fluid shift to intrathoracic airway narrowing in asthma. J. Appl. Physiol. 122(4):809–816, 2017.
Bhatawadekar, S. A., G. Keller, C. O. Francisco, et al. Reduced baseline airway caliber relates to larger airway sensitivity to rostral fluid shift in asthma. Front. Physiol. 8:1012, 2017.
Cao, X., Francisco C. de Oliveira, T. D. Bradley, et al. Association of obstructive apnea with thoracic fluid shift and small airways narrowing in asthma during sleep. Nat. Sci. Sleep. 14:891, 2022.
Cao, X., T. D. Bradley, S. A. Bhatawadekar, et al. Effect of simulated obstructive apnea on thoracic fluid volume and airway narrowing in asthma. Am. J. Respir. Crit. Care Med. 203(7):908–910, 2021.
Oostveen, E., D. MacLeod, H. Lorino, et al. The forced oscillation technique in clinical practice: methodology, recommendations and future developments. Eur. Respir. J. 22(6):1026–1041, 2003.
Prasad, B., S. M. Nyenhuis, I. Imayama, A. Siddiqi, and M. Teodorescu. Asthma and obstructive sleep apnea overlap: what has the evidence taught us? Am. J. Respir. Crit. Care Med. 201(11):1345–1357, 2020.
Bateman, E. D., S. S. Hurd, P. J. Barnes, et al. Global strategy for asthma management and prevention: GINA executive summary. Eur. Respir. J. 31(1):143–178, 2008.
Nathan, R. A., C. A. Sorkness, M. Kosinski, et al. Development of the asthma control test: a survey for assessing asthma control. J. Allergy Clin. Immunol. 113(1):59–65, 2004.
Maddison, K. J., K. L. Shepherd, V. A. Baker, et al. Effects on upper airway collapsibility of presence of a pharyngeal catheter. J. Sleep Res. 24(1):92–99, 2015.
Yadollahi, A., J. M. Gabriel, L. H. White, L. Taranto Montemurro, T. Kasai, and T. D. Bradley. A randomized, double crossover study to investigate the influence of saline infusion on sleep apnea severity in men. Sleep. 37(10):1699–1705, 2014.
Bijaoui, E. L., V. Champagne, P. F. Baconnier, R. J. Kimoff, and J. H. Bates. Mechanical properties of the lung and upper airways in patients with sleep-disordered breathing. Am. J. Respir. Crit. Care Med. 165(8):1055–1061, 2002.
Griscom, N. T., and M. E. B. Wohl. Dimensions of the growing trachea related to body height: length, anteroposterior and transverse diameters, cross-sectional area, and volume in subjects younger than 20 years of age. Am. Rev. Respir. Dis. 131(6):840–844, 1985.
Ge, X., H. Huang, C. Bai, et al. The lengths of trachea and main bronchus in chinese shanghai population. Sci. Rep. 11(1):1–5, 2021.
Eagle, C. The relationship between a person’s height and appropriate endotracheal tube length. Anaesth. Intensive Care. 20(2):156–160, 1992.
Cinar, U., S. Halezeroglu, E. Okur, M. A. Inanici, and S. Kayaoglu. Tracheal length in adult human: The results of 100 autopsies. Int. J. Morphol. 34:232–236, 2016.
McFadden, E. R., Jr., and H. A. Lyons. Arterial-blood gas tension in asthma. N. Engl. J. Med. 278(19):1027–1032, 1968.
Broytman, O., R. K. Braun, B. J. Morgan, et al. Effects of chronic intermittent hypoxia on allergen-induced airway inflammation in rats. Am. J. Respir. Cell Mol. Biol. 52(2):162–170, 2015.
Huxtable, A. G., S. Vinit, J. A. Windelborn, et al. Systemic inflammation impairs respiratory chemoreflexes and plasticity. Respir. Physiol. Neurobiol. 178(3):482–489, 2011.
Prasad, B., S. M. Nyenhuis, and T. E. Weaver. Obstructive sleep apnea and asthma: Associations and treatment implications. Sleep Med. Rev. 18(2):165–171, 2014.
Alkhalil, M., E. Schulman, and J. Getsy. Obstructive sleep apnea syndrome and asthma: what are the links? J. Clin. Sleep Med. 5(1):71–78, 2009.
Aihara, K., T. Oga, Y. Chihara, et al. Analysis of systemic and airway inflammation in obstructive sleep apnea. Sleep Breath. 17:597–604, 2013.
Barnes, P. J., S. Pedersen, and W. W. Busse. Efficacy and safety of inhaled corticosteroids: new developments. Am. J. Respir. Crit. Care Med. 157(3):S1–S53, 1998.
Chung, K. F. Furosemide and other diuretics in asthma. J. Asthma. 31(2):85–92, 1994.
Barnes, P. J. Diuretics and asthma. Thorax. 48(3):195, 1993.
Funding
This study was funded by Ontario Lung Association, Canadian Respiratory Research Network and Ontario Centre of Excellence. NM was supported by a scholarship from Borealis AI and Royal Bank of Canada. TDB was supported by the University of Toronto’s Godfrey S. Pettit Chair in Respiratory Medicine.
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Conception and design: NMG, AY. Formalizing hypothesis: XC, TDB, AY. Patient assessment and recruitment: XC, SMT, MS, KRC. Data acquisition: XC, TDB. Data analysis: NMG. Data interpretation: NMG, XC, TDB, AY. Drafting the manuscript for important intellectual content: NMG, SC. Reviewing manuscript: SC, XC, TDB, SMT, KRC, AY. Approving final version of manuscript for submission: AY.
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Montazeri Ghahjaverestan, N., Chavoshian, S., Cao, X. et al. The Effect of Simulated Obstructive Apneas on Mechanical Characteristics of Lower Airways in Individuals with Asthma. Ann Biomed Eng (2024). https://doi.org/10.1007/s10439-024-03475-3
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DOI: https://doi.org/10.1007/s10439-024-03475-3