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Review Article

The Strain on Airway Smooth Muscle During a Deep Inspiration to Total Lung Capacity

[+] Author and Article Information
Ynuk Bossé

Université Laval,
Faculty of Medicine,
Department of Medicine,
IUCPQ,
M2694, Pavillon Mallet,
Chemin Sainte-Foy,
Québec, QC G1V 4G5, Canada
e-mail: ynuk.bosse@criucpq.ulaval.ca

Manuscript received August 31, 2018; final manuscript received November 6, 2018; published online January 18, 2019. Assoc. Editor: Chun Seow.

ASME J of Medical Diagnostics 2(1), 010802 (Jan 18, 2019) (21 pages) Paper No: JESMDT-18-1046; doi: 10.1115/1.4042309 History: Received August 31, 2018; Revised November 06, 2018

The deep inspiration (DI) maneuver entices a great deal of interest because of its ability to temporarily ease the flow of air into the lungs. This salutary effect of a DI is proposed to be mediated, at least partially, by momentarily increasing the operating length of airway smooth muscle (ASM). Concerningly, this premise is largely derived from a growing body of in vitro studies investigating the effect of stretching ASM by different magnitudes on its contractility. The relevance of these in vitro findings remains uncertain, as the real range of strains ASM undergoes in vivo during a DI is somewhat elusive. In order to understand the regulation of ASM contractility by a DI and to infer on its putative contribution to the bronchodilator effect of a DI, it is imperative that in vitro studies incorporate levels of strains that are physiologically relevant. This review summarizes the methods that may be used in vivo in humans to estimate the strain experienced by ASM during a DI from functional residual capacity (FRC) to total lung capacity (TLC). The strengths and limitations of each method, as well as the potential confounders, are also discussed. A rough estimated range of ASM strains is provided for the purpose of guiding future in vitro studies that aim at quantifying the regulatory effect of DI on ASM contractility. However, it is emphasized that, owing to the many limitations and confounders, more studies will be needed to reach conclusive statements.

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Copyright © 2019 by ASME
Topics: Lung , Muscle , Pressure
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References

Nadel, J. A. , and Tierney, D. F. , 1961, “ Effect of a Previous Deep Inspiration on Airway Resistance in Man,” J. Appl. Physiol., 16, pp. 717–719. [CrossRef] [PubMed]
Skloot, G. , and Togias, A. , 2003, “ Bronchodilation and Bronchoprotection by Deep Inspiration and Their Relationship to Bronchial Hyperresponsiveness,” Clin. Rev. Allergy Immunol., 24(1), pp. 55–72. [CrossRef] [PubMed]
Duggan, C. J. , Chan, J. , Whelan, A. J. , and Berend, N. , 1990, “ Bronchodilatation Induced by Deep Breaths in Relation to Transpulmonary Pressure and Lung Volume,” Thorax, 45(12), pp. 930–934. [CrossRef] [PubMed]
Hida, W. , Arai, M. , Shindoh, C. , Liu, Y. N. , Sasaki, H. , and Takishima, T. , 1984, “ Effect of Inspiratory Flow Rate on Bronchomotor Tone in Normal and Asthmatic Subjects,” Thorax, 39(2), pp. 86–92. [CrossRef] [PubMed]
Salerno, F. G. , Pellegrino, R. , Trocchio, G. , Spanevello, A. , Brusasco, V. , and Crimi, E. , 2005, “ Attenuation of Induced Bronchoconstriction in Healthy Subjects: Effects of Breathing Depth,” J. Appl. Physiol., 98(3), pp. 817–821. [CrossRef] [PubMed]
Melville, K. I. , and Caplan, H. , 1948, “ The Influence of Lung Distension Upon the Response of the Bronchioles to Epinephrine and to Histamine,” J. Pharmacol. Exp. Ther., 94(2), pp. 182–191. http://jpet.aspetjournals.org/content/94/2/182 [PubMed]
Chapman, D. G. , Brown, N. J. , and Salome, C. M. , 2011, “ The Dynamic Face of Respiratory Research: Understanding the Effect of Airway Disease on a Lung in Constant Motion,” Pulm. Pharmacol. Ther., 24(5), pp. 505–512. [CrossRef] [PubMed]
Fredberg, J. J. , 2002, “ Airway Narrowing in Asthma: Does Speed Kill?,” Am. J. Physiol. Lung Cell Mol. Physiol., 283(6), pp. L1179–L1180. [CrossRef] [PubMed]
Lutchen, K. R. , 2014, “ Airway Smooth Muscle Stretch and Airway Hyperresponsiveness in Asthma: Have We Chased the Wrong Horse?,” J. Appl. Physiol., 116(8), pp. 1113–1115. [CrossRef] [PubMed]
Chin, L. Y. , Bosse, Y. , Pascoe, C. , Hackett, T. L. , Seow, C. Y. , and Pare, P. D. , 2012, “ Mechanical Properties of Asthmatic Airway Smooth Muscle,” Eur. Respir. J., 40(1), pp. 45–54. [CrossRef] [PubMed]
Pascoe, C. D. , Seow, C. Y. , Pare, P. D. , and Bosse, Y. , 2013, “ Decrease of Airway Smooth Muscle Contractility Induced by Simulated Breathing Maneuvers Is Not Simply Proportional to Strain,” J. Appl. Physiol., 114(3), pp. 335–343. [CrossRef] [PubMed]
Lavoie, T. L. , Krishnan, R. , Siegel, H. R. , Maston, E. D. , Fredberg, J. J. , Solway, J. , and Dowell, M. L. , 2012, “ Dilatation of the Constricted Human Airway by Tidal Expansion of Lung Parenchyma,” Am. J. Respir. Crit. Care Med., 186(3), pp. 225–232. [CrossRef] [PubMed]
Fredberg, J. J. , Inouye, D. , Miller, B. , Nathan, M. , Jafari, S. , Raboudi, S. H. , Butler, J. P. , and Shore, S. A. , 1997, “ Airway Smooth Muscle, Tidal Stretches, and Dynamically Determined Contractile States,” Am. J. Respir. Crit. Care Med., 156(6), pp. 1752–1759. [CrossRef] [PubMed]
Wang, L. , Pare, P. D. , and Seow, C. Y. , 2000, “ Effects of Length Oscillation on the Subsequent Force Development in Swine Tracheal Smooth Muscle,” J. Appl. Physiol., 88(6), pp. 2246–2250. [CrossRef] [PubMed]
Gump, A. , Haughney, L. , and Fredberg, J. , 2001, “ Relaxation of Activated Airway Smooth Muscle: Relative Potency of Isoproterenol vs. Tidal Stretch,” J. Appl. Physiol., 90(6), pp. 2306–2310. [CrossRef] [PubMed]
Gunst, S. J. , 1983, “ Contractile Force of Canine Airway Smooth Muscle During Cyclical Length Changes,” J. Appl. Physiol., 55(3), pp. 759–769. [CrossRef]
Latourelle, J. , Fabry, B. , and Fredberg, J. J. , 2002, “ Dynamic Equilibration of Airway Smooth Muscle Contraction During Physiological Loading,” J. Appl. Physiol., 92(2), pp. 771–779. [CrossRef] [PubMed]
Raboudi, S. H. , Miller, B. , Butler, J. P. , Shore, S. A. , and Fredberg, J. J. , 1998, “ Dynamically Determined Contractile States of Airway Smooth Muscle,” Am. J. Respir. Crit. Care Med., 158(Pt. 3), pp. S176–S178. [CrossRef] [PubMed]
Oliver, M. N. , Fabry, B. , Marinkovic, A. , Mijailovich, S. M. , Butler, J. P. , and Fredberg, J. J. , 2007, “ Airway Hyperresponsiveness, Remodeling, and Smooth Muscle Mass: Right Answer, Wrong Reason?,” Am. J. Respir. Cell Mol. Biol., 37(3), pp. 264–272. [CrossRef] [PubMed]
Lavoie, T. L. , Dowell, M. L. , Lakser, O. J. , Gerthoffer, W. T. , Fredberg, J. J. , Seow, C. Y. , Mitchell, R. W. , and Solway, J. , 2009, “ Disrupting Actin-Myosin-Actin Connectivity in Airway Smooth Muscle as a Treatment for Asthma?,” Proc. Am. Thorac. Soc., 6(3), pp. 295–300. [CrossRef] [PubMed]
Wang, L. , Pare, P. D. , and Seow, C. Y. , 2001, “ Selected Contribution: Effect of Chronic Passive Length Change on Airway Smooth Muscle Length-Tension Relationship,” J. Appl. Physiol., 90(2), pp. 734–740. [CrossRef] [PubMed]
Noble, P. B. , Jones, R. L. , Needi, E. T. , Cairncross, A. , Mitchell, H. W. , James, A. L. , and McFawn, P. K. , 2011, “ Responsiveness of the Human Airway In Vitro During Deep Inspiration and Tidal Oscillation,” J. Appl. Physiol., 110(6), pp. 1510–1518. [CrossRef] [PubMed]
Noble, P. B. , McFawn, P. K. , and Mitchell, H. W. , 2007, “ Responsiveness of the Isolated Airway During Simulated Deep Inspirations: Effect of Airway Smooth Muscle Stiffness and Strain,” J. Appl. Physiol., 103(3), pp. 787–795. [CrossRef] [PubMed]
Shen, X. , Gunst, S. J. , and Tepper, R. S. , 1997, “ Effect of Tidal Volume and Frequency on Airway Responsiveness in Mechanically Ventilated Rabbits,” J. Appl. Physiol., 83(4), pp. 1202–1208. [CrossRef] [PubMed]
Dowell, M. L. , Lakser, O. J. , Gerthoffer, W. T. , Fredberg, J. J. , Stelmack, G. L. , Halayko, A. J. , Solway, J. , and Mitchell, R. W. , 2005, “ Latrunculin B Increases Force Fluctuation-Induced Relengthening of ACh-Contracted, Isotonically Shortened Canine Tracheal Smooth Muscle,” J. Appl. Physiol., 98(2), pp. 489–497. [CrossRef] [PubMed]
Dowell, M. L. , Lavoie, T. L. , Lakser, O. J. , Dulin, N. O. , Fredberg, J. J. , Gerthoffer, W. T. , Seow, C. Y. , Mitchell, R. W. , and Solway, J. , 2010, “ MEK Modulates Force-Fluctuation-Induced Relengthening of Canine Tracheal Smooth Muscle,” Eur. Respir. J., 36(3), pp. 630–637. [CrossRef] [PubMed]
Lakser, O. J. , Dowell, M. L. , Hoyte, F. L. , Chen, B. , Lavoie, T. L. , Ferreira, C. , Pinto, L. H. , Dulin, N. O. , Kogut, P. , Churchill, J. , Mitchell, R. W. , and Solway, J. , 2008, “ Steroids Augment Relengthening of Contracted Airway Smooth Muscle: Potential Additional Mechanism of Benefit in Asthma,” Eur. Respir. J., 32(5), pp. 1224–1230. [CrossRef] [PubMed]
Noble, P. B. , Jones, R. L. , Cairncross, A. , Elliot, J. G. , Mitchell, H. W. , James, A. L. , and McFawn, P. K. , 2013, “ Airway Narrowing and Bronchodilation to Deep Inspiration in Bronchial Segments From Subjects With and Without Reported Asthma,” J. Appl. Physiol., 114(10), pp. 1460–1471. [CrossRef] [PubMed]
Harvey, B. C. , Parameswaran, H. , and Lutchen, K. R. , 2013, “ Can Tidal Breathing With Deep Inspirations of Intact Airways Create Sustained Bronchoprotection or Bronchodilation?,” J. Appl. Physiol., 115(4), pp. 436–445. [CrossRef] [PubMed]
Ansell, T. K. , McFawn, P. K. , Mitchell, H. W. , and Noble, P. B. , 2013, “ Bronchodilatory Response to Deep Inspiration in Bronchial Segments: The Effects of Stress vs. Strain,” J. Appl. Physiol., 115(4), pp. 505–513. [CrossRef] [PubMed]
Fairbank, N. J. , Connolly, S. C. , Mackinnon, J. D. , Wehry, K. , Deng, L. , and Maksym, G. N. , 2008, “ Airway Smooth Muscle Cell Tone Amplifies Contractile Function in the Presence of Chronic Cyclic Strain,” Am. J. Physiol. Lung Cell Mol. Physiol., 295(3), pp. L479–L488. [CrossRef] [PubMed]
Ijpma, G. , Kachmar, L. , Matusovsky, O. S. , Bates, J. H. , Benedetti, A. , Martin, J. G. , and Lauzon, A. M. , 2015, “ Human Trachealis and Main Bronchi Smooth Muscle Are Normoresponsive in Asthma,” Am. J. Respir. Crit. Care Med., 191(8), pp. 884–893. [CrossRef] [PubMed]
LaPrad, A. S. , Szabo, T. L. , Suki, B. , and Lutchen, K. R. , 2010, “ Tidal Stretches Do Not Modulate Responsiveness of Intact Airways In Vitro,” J. Appl. Physiol., 109(2), pp. 295–304. [CrossRef] [PubMed]
Ansell, T. K. , McFawn, P. K. , Noble, P. B. , West, A. R. , Fernandes, L. , and Mitchell, H. W. , 2009, “ Potent Bronchodilation and Reduced Stiffness by Relaxant Stimuli Under Dynamic Conditions,” Eur. Respir. J., 33(4), pp. 844–851. [CrossRef] [PubMed]
LaPrad, A. S. , West, A. R. , Noble, P. B. , Lutchen, K. R. , and Mitchell, H. W. , 2008, “ Maintenance of Airway Caliber in Isolated Airways by Deep Inspiration and Tidal Strains,” J. Appl. Physiol., 105(2), pp. 479–485. [CrossRef] [PubMed]
Ansell, T. K. , Mitchell, H. W. , McFawn, P. K. , and Noble, P. B. , 2016, “ TNF and IL-1β Exposure Increases Airway Narrowing but Does Not Alter the Bronchodilatory Response to Deep Inspiration in Airway Segments,” Respirology, 21(6), pp. 1041–1048. [CrossRef] [PubMed]
Ansell, T. K. , Noble, P. B. , Mitchell, H. W. , and McFawn, P. K. , 2014, “ Pharmacological Bronchodilation Is Partially Mediated by Reduced Airway Wall Stiffness,” Br. J. Pharmacol., 171(19), pp. 4376–4384.
Ansell, T. K. , Noble, P. B. , Mitchell, H. W. , West, A. R. , Fernandes, L. B. , and McFawn, P. K. , 2009, “ Effects of Simulated Tidal and Deep Breathing on Immature Airway Contraction to Acetylcholine and Nerve Stimulation,” Respirology, 14(7), pp. 991–998. [CrossRef] [PubMed]
Cairncross, A. , Noble, P. B. , and McFawn, P. K. , 2018, “ Hyperinflation of Bronchi In Vitro Impairs Bronchodilation to Simulated Breathing and Increases Sensitivity to Contractile Activation,” Respirology, 23(8), pp. 750–755. [CrossRef] [PubMed]
Harvey, B. C. , Parameswaran, H. , and Lutchen, K. R. , 2015, “ Can Breathing-Like Pressure Oscillations Reverse or Prevent Narrowing of Small Intact Airways?,” J. Appl. Physiol., 119(1), pp. 47–54. [CrossRef] [PubMed]
Chin, L. Y. , Bosse, Y. , Jiao, Y. , Solomon, D. , Hackett, T. L. , Pare, P. D. , and Seow, C. Y. , 2010, “ Human Airway Smooth Muscle is Structurally and Mechanically Similar to That of Other Species,” Eur. Respir. J., 36(1), pp. 170–177. [CrossRef] [PubMed]
Gunst, S. J. , and Lai-Fook, S. J. , 1983, “ Effect of Inflation on Trachealis Muscle Tone in Canine Tracheal Segments In Vitro,” J. Appl. Physiol., 54(4), pp. 906–913. [CrossRef]
Gunst, S. J. , and Stropp, J. Q. , 1988, “ Pressure-Volume and Length-Stress Relationships in Canine Bronchi In Vitro,” J. Appl. Physiol., 64(6), pp. 2522–2531. [CrossRef] [PubMed]
Gunst, S. J. , Stropp, J. Q. , and Service, J. , 1990, “ Mechanical Modulation of Pressure-Volume Characteristics of Contracted Canine Airways In Vitro,” J. Appl. Physiol., 68(5), pp. 2223–2229. [CrossRef] [PubMed]
Mitchell, R. W. , Dowell, M. L. , Solway, J. , and Lakser, O. J. , 2008, “ Force Fluctuation Induced Relengthening of Acetylcholine-Contracted Airway Smooth Muscle,” Proc. Am. Thorac. Soc., 5(1), pp. 68–72. [CrossRef] [PubMed]
Mailhot-Larouche, S. , Lortie, K. , Marsolais, D. , Flamand, N. , and Bosse, Y. , 2017, “ An In Vitro Study Examining the Duration Between Deep Inspirations on the Rate of Renarrowing,” Respir. Physiol. Neurobiol., 243, pp. 13–19. [CrossRef] [PubMed]
Gazzola, M. , Henry, C. , Couture, C. , Marsolais, D. , King, G. G. , Fredberg, J. J. , and Bosse, Y. , 2016, “ Smooth Muscle in Human Bronchi Is Disposed to Resist Airway Distension,” Respir. Physiol. Neurobiol., 229, pp. 51–58. [CrossRef] [PubMed]
Wang, L. , Chitano, P. , and Murphy, T. M. , 2005, “ Length Oscillation Induces Force Potentiation in Infant Guinea Pig Airway Smooth Muscle,” Am. J. Physiol. Lung Cell Mol. Physiol., 289(6), pp. L909–L915. [CrossRef] [PubMed]
Fowler, W. S. , 1948, “ Lung Function Studies; the Respiratory Dead Space,” Am. J. Physiol., 154(3), pp. 405–416. [PubMed]
Carter, E. T. , Gray, J. S. , and Grodins, F. S. , 1956, “ Alveolar and Total Ventilation and the Dead Space Problem,” J. Appl. Physiol., 9(3), pp. 307–320. [CrossRef] [PubMed]
Shepard, R. H. , Campbell, E. J. , Martin, H. B. , and Enns, T. , 1957, “ Factors Affecting the Pulmonary Dead Space as Determined by Single Breath Analysis,” J. Appl. Physiol., 11(2), pp. 241–244. [CrossRef] [PubMed]
Briscoe, W. A. , and Dubois, A. B. , 1958, “ The Relationship Between Airway Resistance, Airway Conductance and Lung Volume in Subjects of Different Age and Body Size,” J. Clin. Invest., 37(9), pp. 1279–1285. [CrossRef] [PubMed]
Birath, G. , 1959, “ Respiratory Dead Space Measurements in a Model Lung and Healthy Human Subjects According to the Single Breath Method,” J. Appl. Physiol., 14(4), pp. 517–520. [CrossRef]
Butler, J. , Caro, C. G. , Alcala, R. , and Dubois, A. B. , 1960, “ Physiological Factors Affecting Airway Resistance in Normal Subjects and in Patients With Obstructive Respiratory Disease,” J. Clin. Invest., 39(4), pp. 584–591. [CrossRef] [PubMed]
Marshall, R. , and Holden, W. S. , 1963, “ Changes in Calibre of the Smaller Airways in Man,” Thorax, 18(1), pp. 54–58. [CrossRef]
Blide, R. W. , Kerr, H. D. , and Spicer, W. S., Jr. , 1964, “ Measurement of Upper and Lower Airway Resistance and Conductance in Man,” J. Appl. Physiol., 19, pp. 1059–1069. [CrossRef] [PubMed]
Froeb, H. F. , and Mead, J. , 1968, “ Relative Hysteresis of the Dead Space and Lung In Vivo,” J. Appl. Physiol., 25(3), pp. 244–248. [CrossRef] [PubMed]
Vincent, N. J. , Knudson, R. , Leith, D. E. , Macklem, P. T. , and Mead, J. , 1970, “ Factors Influencing Pulmonary Resistance,” J. Appl. Physiol., 29(2), pp. 236–243. [CrossRef] [PubMed]
Colebatch, H. J. , Finucane, K. E. , and Smith, M. M. , 1973, “ Pulmonary Conductance and Elastic Recoil Relationships in Asthma and Emphysema,” J. Appl. Physiol., 34(2), pp. 143–153. [CrossRef] [PubMed]
Johnson, T. H. , Mikita, J. J. , Wilson, R. J. , and Feist, J. H. , 1973, “ Acquired Tracheomalacia,” Radiology, 109(3), pp. 576–580. [CrossRef] [PubMed]
Dolyniuk, M. V. , and Fahey, P. J. , 1986, “ Relationship of Tracheal Size to Maximal Expiratory Airflow and Density Dependence,” J. Appl. Physiol., 60(2), pp. 501–505. [CrossRef] [PubMed]
Hoffstein, V. , Castile, R. G. , O'Donnell, C. R. , Glass, G. M. , Strieder, D. J. , Wohl, M. E. , and Fredberg, J. J. , 1987, “ In Vivo Estimation of Tracheal Distensibility and Hysteresis in Normal Adults,” J. Appl. Physiol., 63(6), pp. 2482–2489. [CrossRef] [PubMed]
Brooks, L. J. , 1990, “ Tracheal Size and Distensibility in Patients With Cystic Fibrosis,” Am. Rev. Respir. Dis., 141(2), pp. 513–516. [CrossRef] [PubMed]
Wilson, J. W. , Li, X. , and Pain, M. C. , 1993, “ The Lack of Distensibility of Asthmatic Airways,” Am. Rev. Respir. Dis., 148(3), pp. 806–809. [CrossRef] [PubMed]
Suto, Y. , and Tanabe, Y. , 1998, “ Evaluation of Tracheal Collapsibility in Patients With Tracheomalacia Using Dynamic MR Imaging During Coughing,” Am. J. Roentgenol., 171(2), pp. 393–394. [CrossRef]
Brackel, H. J. , Pedersen, O. F. , Mulder, P. G. , Overbeek, S. E. , Kerrebijn, K. F. , and Bogaard, J. M. , 2000, “ Central Airways Behave More Stiffly During Forced Expiration in Patients With Asthma,” Am. J. Respir. Crit. Care Med., 162(3 Pt. 1), pp. 896–904. [CrossRef] [PubMed]
Johns, D. P. , Wilson, J. , Harding, R. , and Walters, E. H. , 2000, “ Airway Distensibility in Healthy and Asthmatic Subjects: Effect of Lung Volume History,” J. Appl. Physiol., 88(4), pp. 1413–1420. [CrossRef] [PubMed]
Brown, R. H. , Scichilone, N. , Mudge, B. , Diemer, F. B. , Permutt, S. , and Togias, A. , 2001, “ High-Resolution Computed Tomographic Evaluation of Airway Distensibility and the Effects of Lung Inflation on Airway Caliber in Healthy Subjects and Individuals With Asthma,” Am. J. Respir. Crit. Care Med., 163(4), pp. 994–1001. [CrossRef] [PubMed]
Ward, C. , Johns, D. P. , Bish, R. , Pais, M. , Reid, D. W. , Ingram, C. , Feltis, B. , and Walters, E. H. , 2001, “ Reduced Airway Distensibility, Fixed Airflow Limitation, and Airway Wall Remodeling in Asthma,” Am. J. Respir. Crit. Care Med., 164(9), pp. 1718–1721. [CrossRef] [PubMed]
Jensen, A. , Atileh, H. , Suki, B. , Ingenito, E. P. , and Lutchen, K. R. , 2001, “ Selected Contribution: Airway Caliber in Healthy and Asthmatic Subjects: Effects of Bronchial Challenge and Deep Inspirations,” J. Appl. Physiol., 91(1), pp. 506–515. [CrossRef] [PubMed]
Black, L. D. , Dellaca, R. , Jung, K. , Atileh, H. , Israel, E. , Ingenito, E. P. , and Lutchen, K. R. , 2003, “ Tracking Variations in Airway Caliber by Using Total Respiratory vs. Airway Resistance in Healthy and Asthmatic Subjects,” J. Appl. Physiol., 95(2), pp. 511–518. [CrossRef] [PubMed]
Salome, C. M. , Thorpe, C. W. , Diba, C. , Brown, N. J. , Berend, N. , and King, G. G. , 2003, “ Airway Re-Narrowing Following Deep Inspiration in Asthmatic and Nonasthmatic Subjects,” Eur. Respir. J., 22(1), pp. 62–68. [CrossRef] [PubMed]
Brown, N. J. , Thorpe, C. W. , Thompson, B. , Berend, N. , Downie, S. , Verbanck, S. , Salome, C. M. , and King, G. G. , 2004, “ A Comparison of Two Methods for Measuring Airway Distensibility: Nitrogen Washout and the Forced Oscillation Technique,” Physiol. Meas., 25(4), pp. 1067–1075. [CrossRef] [PubMed]
Baroni, R. H. , Feller-Kopman, D. , Nishino, M. , Hatabu, H. , Loring, S. H. , Ernst, A. , and Boiselle, P. M. , 2005, “ Tracheobronchomalacia: Comparison Between End-Expiratory and Dynamic Expiratory CT for Evaluation of Central Airway Collapse,” Radiology, 235(2), pp. 635–641. [CrossRef] [PubMed]
Brown, N. J. , Salome, C. M. , Berend, N. , Thorpe, C. W. , and King, G. G. , 2007, “ Airway Distensibility in Adults With Asthma and Healthy Adults, Measured by Forced Oscillation Technique,” Am. J. Respir. Crit. Care Med., 176(2), pp. 129–137. [CrossRef] [PubMed]
Scichilone, N. , La Sala, A. , Bellia, M. , Fallano, K. , Togias, A. , Brown, R. H. , Midiri, M. , and Bellia, V. , 2008, “ The Airway Response to Deep Inspirations Decreases With COPD Severity and Is Associated With Airway Distensibility Assessed by Computed Tomography,” J. Appl. Physiol., 105(3), pp. 832–838. [CrossRef] [PubMed]
Matsuoka, S. , Kurihara, Y. , Yagihashi, K. , Hoshino, M. , and Nakajima, Y. , 2008, “ Airway Dimensions at Inspiratory and Expiratory Multisection CT in Chronic Obstructive Pulmonary Disease: Correlation With Airflow Limitation,” Radiology, 248(3), pp. 1042–1049. [CrossRef] [PubMed]
Ferretti, G. R. , Jankowski, A. , Perrin, M. A. , Chouri, N. , Arnol, N. , Aubaud, L. , and Pepin, J. L. , 2008, “ Multi-Detector CT Evaluation in Patients Suspected of Tracheobronchomalacia: Comparison of End-Expiratory With Dynamic Expiratory Volumetric Acquisitions,” Eur. J. Radiol., 68(2), pp. 340–346. [CrossRef] [PubMed]
McDermott, S. , Barry, S. C. , Judge, E. E. , Collins, S. , de Jong, P. A. , Tiddens, H. A. , McKone, E. F. , Gallagher, C. C. , and Dodd, J. D. , 2009, “ Tracheomalacia in Adults With Cystic Fibrosis: Determination of Prevalence and Severity With Dynamic Cine CT,” Radiology, 252(2), pp. 577–586. [CrossRef] [PubMed]
Kelly, V. J. , Brown, N. J. , King, G. G. , and Thompson, B. R. , 2010, “ A Method to Determine In Vivo, Specific Airway Compliance, in Humans,” Med. Biol. Eng. Comput., 48(5), pp. 489–496. [CrossRef] [PubMed]
Baldi, S. , Dellaca, R. , Govoni, L. , Torchio, R. , Aliverti, A. , Pompilio, P. , Corda, L. , Tantucci, C. , Gulotta, C. , Brusasco, V. , and Pellegrino, R. , 2010, “ Airway Distensibility and Volume Recruitment With Lung Inflation in COPD,” J. Appl. Physiol., 109(4), pp. 1019–1026. [CrossRef] [PubMed]
Kermode, J. A. , Brown, N. J. , Hardaker, K. M. , Farah, C. S. , Berend, N. , King, G. G. , and Salome, C. M. , 2011, “ The Effect of Airway Remodelling on Airway Hyper-Responsiveness in Asthma,” Respir. Med., 105(12), pp. 1798–1804. [CrossRef] [PubMed]
Mendonca, N. T. , Kenyon, J. , LaPrad, A. S. , Syeda, S. N. , O'Connor, G. T. , and Lutchen, K. R. , 2011, “ Airway Resistance at Maximum Inhalation as a Marker of Asthma and Airway Hyperresponsiveness,” Respir. Res., 12, p. 96. [CrossRef] [PubMed]
Kelly, V. J. , Brown, N. J. , King, G. G. , and Thompson, B. R. , 2011, “ The Bronchodilator Response of In Vivo Specific Airway Compliance in Adults With Asthma,” Ann. Biomed. Eng., 39(3), pp. 1125–1135. [CrossRef] [PubMed]
Williamson, J. P. , McLaughlin, R. A. , Noffsinger, W. J. , James, A. L. , Baker, V. A. , Curatolo, A. , Armstrong, J. J. , Regli, A. , Shepherd, K. L. , Marks, G. B. , Sampson, D. D. , Hillman, D. R. , and Eastwood, P. R. , 2011, “ Elastic Properties of the Central Airways in Obstructive Lung Diseases Measured Using Anatomical Optical Coherence Tomography,” Am. J. Respir. Crit. Care Med., 183(5), pp. 612–619. [CrossRef] [PubMed]
Pyrgos, G. , Scichilone, N. , Togias, A. , and Brown, R. H. , 2011, “ Bronchodilation Response to Deep Inspirations in Asthma is Dependent on Airway Distensibility and Air Trapping,” J. Appl. Physiol., 110(2), pp. 472–479. [CrossRef] [PubMed]
Bakker, M. E. , Stolk, J. , Reiber, J. H. , and Stoel, B. C. , 2012, “ Influence of Inspiration Level on Bronchial Lumen Measurements With Computed Tomography,” Respir. Med., 106(5), pp. 677–686. [CrossRef] [PubMed]
Diaz, A. A. , Come, C. E. , Ross, J. C. , San Jose Estepar, R. , Han, M. K. , Loring, S. H. , Silverman, E. K. , and Washko, G. R. , 2012, “ Association Between Airway Caliber Changes With Lung Inflation and Emphysema Assessed by Volumetric CT Scan in Subjects With COPD,” Chest, 141(3), pp. 736–744. [CrossRef] [PubMed]
Leboulanger, N. , Louis, B. , Corvol, H. , Ramirez, A. , Fodil, R. , Lofaso, F. , and Fauroux, B. , 2012, “ Evaluation of the Trachea and Intrathoracic Airways by the Acoustic Reflection Method in Children With Cystic Fibrosis,” Respir. Physiol. Neurobiol., 181(1), pp. 74–78. [CrossRef] [PubMed]
Barisione, G. , Pompilio, P. P. , Bacigalupo, A. , Brusasco, C. , Cioe, A. , Dellaca, R. L. , Lamparelli, T. , Garlaschi, A. , Pellegrino, R. , and Brusasco, V. , 2012, “ Airway Distensibility With Lung Inflation After Allogeneic Haematopoietic Stem-Cell Transplantation,” Respir. Physiol. Neurobiol., 184(1), pp. 80–85. [CrossRef] [PubMed]
Benfante, A. , Bellia, M. , Scichilone, N. , Cannizzaro, F. , Midiri, M. , Brown, R. , and Bellia, V. , 2013, “ Airway Distensibility by HRCT in Asthmatics and COPD With Comparable Airway Obstruction,” COPD, 10(5), pp. 560–566. [CrossRef] [PubMed]
Petersen, J. , Wille, M. M. , Raket, L. L. , Feragen, A. , Pedersen, J. H. , Nielsen, M. , Dirksen, A. , and de Bruijne, M. , 2014, “ Effect of Inspiration on Airway Dimensions Measured in Maximal Inspiration CT Images of Subjects Without Airflow Limitation,” Eur. Radiol., 24(9), pp. 2319–2325. [CrossRef] [PubMed]
Adam, R. J. , Hisert, K. B. , Dodd, J. D. , Grogan, B. , Launspach, J. L. , Barnes, J. K. , Gallagher, C. G. , Sieren, J. P. , Gross, T. J. , Fischer, A. J. , Cavanaugh, J. E. , Hoffman, E. A. , Singh, P. K. , Welsh, M. J. , McKone, E. F. , and Stoltz, D. A. , 2016, “ Acute Administration of Ivacaftor to People With Cystic Fibrosis and a G551D-CFTR Mutation Reveals Smooth Muscle Abnormalities,” JCI Insight, 1(4), p. e86183. [CrossRef] [PubMed]
Brown, R. H. , and Togias, A. , 2016, “ Measurement of Intraindividual Airway Tone Heterogeneity and Its Importance in Asthma,” J. Appl. Physiol., 121(1), pp. 223–232. [CrossRef] [PubMed]
Mailhot-Larouche, S. , Lachance, M. , Bullone, M. , Henry, C. , Dandurand, R. J. , Boulet, L. P. , Laviolette, M. , King, G. G. , Farah, C. S. , and Bosse, Y. , 2017, “ Assessment of Airway Distensibility by the Forced Oscillation Technique: Reproducible and Potentially Simplifiable,” Front. Physiol., 8, p. 223. [CrossRef] [PubMed]
Montesantos, S. , Katz, I. , Venegas, J. , Pichelin, M. , and Caillibotte, G. , 2017, “ The Effect of Disease and Respiration on Airway Shape in Patients With Moderate Persistent Asthma,” PLoS One, 12(7), p. e0182052. [CrossRef] [PubMed]
Smiley-Jewell, S. M. , Tran, M. U. , Weir, A. J. , Johnson, Z. A. , Van Winkle, L. S. , and Plopper, C. G. , 2002, “ Three-Dimensional Mapping of Smooth Muscle in the Distal Conducting Airways of Mouse, Rabbit, and Monkey,” J. Appl. Physiol., 93(4), pp. 1506–1514. [CrossRef] [PubMed]
Ijpma, G. , Panariti, A. , Lauzon, A. M. , and Martin, J. G. , 2017, “ Directional Preference of Airway Smooth Muscle Mass Increase in Human Asthmatic Airways,” Am. J. Physiol. Lung Cell Mol. Physiol., 312(6), pp. L845–L854.
Marthan, R. , and Woolcock, A. J. , 1989, “ Is a Myogenic Response Involved in Deep Inspiration-Induced Bronchoconstriction in Asthmatics?,” Am. Rev. Respir. Dis., 140(5), pp. 1354–1358. [CrossRef] [PubMed]
Wong, R. S. , Larcombe, A. N. , Fernandes, L. B. , Zosky, G. R. , and Noble, P. B. , 2012, “ The Mechanism of Deep Inspiration-Induced Bronchoprotection: Evidence From a Mouse Model,” Eur. Respir. J., 40(4), pp. 982–989. [CrossRef] [PubMed]
Crimi, E. , Pellegrino, R. , Milanese, M. , and Brusasco, V. , 2002, “ Deep Breaths, Methacholine, and Airway Narrowing in Healthy and Mild Asthmatic Subjects,” J. Appl. Physiol., 93(4), pp. 1384–1390. [CrossRef] [PubMed]
Noble, P. B. , McFawn, P. K. , and Mitchell, H. W. , 2004, “ Intraluminal Pressure Oscillation Enhances Subsequent Airway Contraction in Isolated Bronchial Segments,” J. Appl. Physiol., 96(3), pp. 1161–1165. [CrossRef] [PubMed]
Trepat, X. , Deng, L. , An, S. S. , Navajas, D. , Tschumperlin, D. J. , Gerthoffer, W. T. , Butler, J. P. , and Fredberg, J. J. , 2007, “ Universal Physical Responses to Stretch in the Living Cell,” Nature, 447(7144), pp. 592–595. [CrossRef] [PubMed]
Smith, P. G. , Roy, C. , Fisher, S. , Huang, Q. Q. , and Brozovich, F. , 2000, “ Selected Contribution: Mechanical Strain Increases Force Production and Calcium Sensitivity in Cultured Airway Smooth Muscle Cells,” J. Appl. Physiol., 89(5), pp. 2092–2098. [CrossRef] [PubMed]
Smith, P. G. , Roy, C. , Dreger, J. , and Brozovich, F. , 1999, “ Mechanical Strain Increases Velocity and Extent of Shortening in Cultured Airway Smooth Muscle Cells,” Am. J. Physiol., 277(2 Pt 1), pp. L343–L348. [PubMed]
Deng, L. , Fairbank, N. J. , Cole, D. J. , Fredberg, J. J. , and Maksym, G. N. , 2005, “ Airway Smooth Muscle Tone Modulates Mechanically Induced Cytoskeletal Stiffening and Remodeling,” J. Appl. Physiol., 99(2), pp. 634–641. [CrossRef] [PubMed]
Krishnan, R. , Park, C. Y. , Lin, Y. C. , Mead, J. , Jaspers, R. T. , Trepat, X. , Lenormand, G. , Tambe, D. , Smolensky, A. V. , Knoll, A. H. , Butler, J. P. , and Fredberg, J. J. , 2009, “ Reinforcement Versus Fluidization in Cytoskeletal Mechanoresponsiveness,” PLoS One, 4(5), p. e5486. [CrossRef] [PubMed]
Krogh, A. , and Lindhard, J. , 1917, “ The Volume of the Dead Space in Breathing and the Mixing of Gases in the Lungs of Man,” J. Physiol., 51(1–2), pp. 59–90. [CrossRef] [PubMed]
Martin, C. J. , Das, S. , and Young, A. C. , 1979, “ Measurements of the Dead Space Volume,” J. Appl. Physiol.: Respir., Environ. Exercise Physiol., 47(2), pp. 319–324.
Garcia, G. , Perez, T. , and Verbanck, S. , 2012, “ Functional Measurements of the Peripheral Airways in COPD,” Rev. Mal. Respir., 29(2), pp. 319–327. [CrossRef] [PubMed]
Boeck, L. , Gensmer, A. , Nyilas, S. , Stieltjes, B. , Re, T. J. , Tamm, M. , Latzin, P. , and Stolz, D. , 2016, “ Single-Breath Washout Tests to Assess Small Airway Disease in COPD,” Chest, 150(5), pp. 1091–1100. [CrossRef] [PubMed]
Griscom, N. T. , Vawter, G. F. , and Stigol, L. C. , 1987, “ Radiologic and Pathologic Abnormalities of the Trachea in Older Patients With Cystic Fibrosis,” Am. J. Roentgenol., 148(4), pp. 691–693. [CrossRef]
Criee, C. P. , Sorichter, S. , Smith, H. J. , Kardos, P. , Merget, R. , Heise, D. , Berdel, D. , Kohler, D. , Magnussen, H. , Marek, W. , Mitfessel, H. , Rasche, K. , Rolke, M. , Worth, H. , Jorres, R. A. , and Working Group for Body Plethysmography of the German Society for Pneumology and Respiratory Care, 2011, “ Body Plethysmography—Its Principles and Clinical Use,” Respir. Med., 105(7), pp. 959–971. [CrossRef] [PubMed]
Kariya, S. T. , Thompson, L. M. , Ingenito, E. P. , and Ingram, R. H., Jr. , 1989, “ Effects of Lung Volume, Volume History, and Methacholine on Lung Tissue Viscance,” J. Appl. Physiol., 66(2), pp. 977–982. [CrossRef] [PubMed]
Hoffstein, V. , and Zamel, N. , 1984, “ Tracheal Stenosis Measured by the Acoustic Reflection Technique,” Am. Rev. Respir. Dis., 130(3), pp. 472–475. [PubMed]
Fredberg, J. J. , Wohl, M. E. , Glass, G. M. , and Dorkin, H. L. , 1980, “ Airway Area by Acoustic Reflections Measured at the Mouth,” J. Appl. Physiol.: Respir., Environ. Exercise Physiol., 48(5), pp. 749–758.
Brooks, L. J. , Castile, R. G. , Glass, G. M. , Griscom, N. T. , Wohl, M. E. , and Fredberg, J. J. , 1984, “ Reproducibility and Accuracy of Airway Area by Acoustic Reflection,” J. Appl. Physiol.: Respir., Environ. Exercise Physiol., 57(3), pp. 777–787.
de Lange, E. E. , Altes, T. A. , Patrie, J. T. , Battiston, J. J. , Juersivich, A. P. , Mugler , J. P., III , and Platts-Mills, T. A. , 2009, “ Changes in Regional Airflow Obstruction Over Time in the Lungs of Patients With Asthma: Evaluation With 3He MR Imaging,” Radiology, 250(2), pp. 567–575. [CrossRef] [PubMed]
de Lange, E. E. , Altes, T. A. , Patrie, J. T. , Parmar, J. , Brookeman, J. R. , Mugler , J. P., III , and Platts-Mills, T. A. , 2007, “ The Variability of Regional Airflow Obstruction Within the Lungs of Patients With Asthma: Assessment With Hyperpolarized Helium-3 Magnetic Resonance Imaging,” J. Allergy Clin. Immunol., 119(5), pp. 1072–1078. [CrossRef] [PubMed]
Tzeng, Y. S. , Lutchen, K. , and Albert, M. , 2009, “ The Difference in Ventilation Heterogeneity Between Asthmatic and Healthy Subjects Quantified Using Hyperpolarized 3He MRI,” J. Appl. Physiol., 106(3), pp. 813–822. [CrossRef] [PubMed]
Samee, S. , Altes, T. , Powers, P. , de Lange, E. E. , Knight-Scott, J. , Rakes, G. , Mugler , J. P., III , Ciambotti, J. M. , Alford, B. A. , Brookeman, J. R. , and Platts-Mills, T. A. , 2003, “ Imaging the Lungs in Asthmatic Patients by Using Hyperpolarized Helium-3 Magnetic Resonance: Assessment of Response to Methacholine and Exercise Challenge,” J. Allergy Clin. Immunol., 111(6), pp. 1205–1211. [CrossRef] [PubMed]
Campana, L. , Kenyon, J. , Zhalehdoust-Sani, S. , Tzeng, Y. S. , Sun, Y. , Albert, M. , and Lutchen, K. R. , 2009, “ Probing Airway Conditions Governing Ventilation Defects in Asthma Via Hyperpolarized MRI Image Functional Modeling,” J. Appl. Physiol., 106(4), pp. 1293–1300. [CrossRef] [PubMed]
Lewis, T. A. , Tzeng, Y. S. , McKinstry, E. L. , Tooker, A. C. , Hong, K. , Sun, Y. , Mansour, J. , Handler, Z. , and Albert, M. S. , 2005, “ Quantification of Airway Diameters and 3D Airway Tree Rendering From Dynamic Hyperpolarized 3He Magnetic Resonance Imaging,” Magn. Reson. Med., 53(2), pp. 474–478. [CrossRef] [PubMed]
Tzeng, Y. S. , Hoffman, E. , Cook-Granroth, J. , Gereige, J. , Mansour, J. , Washko, G. , Cho, M. , Stepp, E. , Lutchen, K. , and Albert, M. , 2008, “ Investigation of Hyperpolarized 3He Magnetic Resonance Imaging Utility in Examining Human Airway Diameter Behavior in Asthma Through Comparison With High-Resolution Computed Tomography,” Acad. Radiol., 15(6), pp. 799–808. [CrossRef] [PubMed]
Bates, J. H. , Irvin, C. G. , Farre, R. , and Hantos, Z. , 2011, “ Oscillation Mechanics of the Respiratory System,” Compr. Physiol., 1(3), pp. 1233–1272. [PubMed]
Coxson, H. O. , Eastwood, P. R. , Williamson, J. P. , and Sin, D. D. , 2011, “ Phenotyping Airway Disease With Optical Coherence Tomography,” Respirology, 16(1), pp. 34–43. [CrossRef] [PubMed]
Adams, D. C. , Hariri, L. P. , Miller, A. J. , Wang, Y. , Cho, J. L. , Villiger, M. , Holz, J. A. , Szabari, M. V. , Hamilos, D. L. , Scott Harris, R. , Griffith, J. W. , Bouma, B. E. , Luster, A. D. , Medoff, B. D. , and Suter, M. J. , 2016, “ Birefringence Microscopy Platform for Assessing Airway Smooth Muscle Structure and Function In Vivo,” Sci. Transl. Med., 8(359), p. 359ra131. [CrossRef] [PubMed]
Macklin, C. C. , 1925, “ X-Ray Studies on Bronchial Movements,” Am. J. Anat., 35(2), pp. 303–329. [CrossRef]
Hughes, J. M. , Hoppin , F. G., Jr. , and Mead, J. , 1972, “ Effect of Lung Inflation on Bronchial Length and Diameter in Excised Lungs,” J. Appl. Physiol., 32(1), pp. 25–35. [CrossRef] [PubMed]
Brown, R. H. , and Mitzner, W. , 1996, “ Effect of Lung Inflation and Airway Muscle Tone on Airway Diameter In Vivo,” J. Appl. Physiol., 80(5), pp. 1581–1588. [CrossRef] [PubMed]
Klingele, T. G. , and Staub, N. C. , 1971, “ Terminal Bronchiole Diameter Changes With Volume in Isolated, Air-Filled Lobes of Cat Lung,” J. Appl. Physiol., 30(2), pp. 224–227. [CrossRef] [PubMed]
Sasaki, H. , and Hoppin, F. G., Jr. , 1979, “ Hysteresis of Contracted Airway Smooth Muscle,” J. Appl. Physiol.: Respir., Environ. Exercise Physiol., 47(6), pp. 1251–1262.
Khangure, S. R. , Noble, P. B. , Sharma, A. , Chia, P. Y. , McFawn, P. K. , and Mitchell, H. W. , 2004, “ Cyclical Elongation Regulates Contractile Responses of Isolated Airways,” J. Appl. Physiol., 97(3), pp. 913–919. [CrossRef] [PubMed]
Hoffstein, V. , Zamel, N. , and Phillipson, E. A. , 1984, “ Lung Volume Dependence of Pharyngeal Cross-Sectional Area in Patients With Obstructive Sleep Apnea,” Am. Rev. Respir. Dis., 130(2), pp. 175–178. [CrossRef] [PubMed]
Jackson, A. C. , and Krevans, J. R., Jr. , 1984, “ Tracheal Cross-Sectional Areas From Acoustic Reflections in Dogs,” J. Appl. Physiol.: Respir., Environ. Exercise Physiol., 57(2), pp. 351–353.
Lutchen, K. R. , and Gillis, H. , 1997, “ Relationship Between Heterogeneous Changes in Airway Morphometry and Lung Resistance and Elastance,” J. Appl. Physiol., 83(4), pp. 1192–1201. [CrossRef] [PubMed]
Lutchen, K. R. , Hantos, Z. , Petak, F. , Adamicza, A. , and Suki, B. , 1996, “ Airway Inhomogeneities Contribute to Apparent Lung Tissue Mechanics During Constriction,” J. Appl. Physiol., 80(5), pp. 1841–1849. [CrossRef] [PubMed]
Lutchen, K. R. , Jensen, A. , Atileh, H. , Kaczka, D. W. , Israel, E. , Suki, B. , and Ingenito, E. P. , 2001, “ Airway Constriction Pattern is a Central Component of Asthma Severity: The Role of Deep Inspirations,” Am. J. Respir. Crit. Care Med., 164(2), pp. 207–215. [CrossRef] [PubMed]
Hulme, K. M. , Salome, C. M. , Brown, N. J. , Berend, N. , Agus, H. M. , Horlyck, K. R. , King, G. G. , and Chapman, D. G. , 2013, “ Deep Inspiration Volume and the Impaired Reversal of Bronchoconstriction in Asthma,” Respir. Physiol. Neurobiol., 189(3), pp. 506–512. [CrossRef] [PubMed]
Bates, J. H., 2009, “The Linear Single-Compartement Model,” Lung Mechanics: An Inverse Modeling Approach, Cambridge University Press, New York, pp. 37–61.
Wilson, A. G. , Massarella, G. R. , and Pride, N. B. , 1974, “ Elastic Properties of Airways in Human Lungs Post Mortem,” Am. Rev. Respir. Dis., 110(6), pp. 716–729. [PubMed]
Hiorns, J. E. , Jensen, O. E. , and Brook, B. S. , 2014, “ Nonlinear Compliance Modulates Dynamic Bronchoconstriction in a Multiscale Airway Model,” Biophys. J., 107(12), pp. 3030–3042. [CrossRef] [PubMed]
Olsen, C. R. , Stevens, A. E. , and McIlroy, M. B. , 1967, “ Rigidity of Tracheae and Bronchi During Muscular Constriction,” J. Appl. Physiol., 23(1), pp. 27–34. [CrossRef] [PubMed]
Beaupre, A. , and Orehek, J. , 1982, “ Factors Influencing the Bronchodilator Effect of a Deep Inspiration in Asthmatic Patients With Provoked Bronchoconstriction,” Thorax, 37(2), pp. 124–128. [CrossRef] [PubMed]
Gunst, S. J. , and Mitzner, W. , 1981, “ Mechanical Properties of Contracted Canine Bronchial Segments In Vitro,” J. Appl. Physiol., 50(6), pp. 1236–1247. [CrossRef]
Orehek, J. , Nicoli, M. M. , Delpierre, S. , and Beaupre, A. , 1981, “ Influence of the Previous Deep Inspiration on the Spirometric Measurement of Provoked Bronchoconstriction in Asthma,” Am. Rev. Respir. Dis., 123(3), pp. 269–272. https://www.atsjournals.org/doi/abs/10.1164/arrd.1981.123.3.269 [PubMed]
Scichilone, N. , Kapsali, T. , Permutt, S. , and Togias, A. , 2000, “ Deep Inspiration-Induced Bronchoprotection is Stronger Than Bronchodilation,” Am. J. Respir. Crit. Care Med., 162(3 Pt. 1), pp. 910–916. [CrossRef] [PubMed]
Malmberg, P. , Larsson, K. , Sundblad, B. M. , and Zhiping, W. , 1993, “ Importance of the Time Interval Between FEV1 Measurements in a Methacholine Provocation Test,” Eur. Respir. J., 6(5), pp. 680–686. https://journal.chestnet.org/article/S0012-3692(16)47463-5/fulltext [PubMed]
King, G. G. , Moore, B. J. , Seow, C. Y. , and Pare, P. D. , 1999, “ Time Course of Increased Airway Narrowing Caused by Inhibition of Deep Inspiration During Methacholine Challenge,” Am. J. Respir. Crit. Care Med., 160(2), pp. 454–457. [CrossRef] [PubMed]
Kapsali, T. , Permutt, S. , Laube, B. , Scichilone, N. , and Togias, A. , 2000, “ Potent Bronchoprotective Effect of Deep Inspiration and Its Absence in Asthma,” J. Appl. Physiol., 89(2), pp. 711–720. [CrossRef] [PubMed]
Weist, A. , Williams, T. , Kisling, J. , Clem, C. , and Tepper, R. S. , 2002, “ Volume History and Effect on Airway Reactivity in Infants and Adults,” J. Appl. Physiol., 93(3), pp. 1069–1074. [CrossRef] [PubMed]
King, G. G. , Moore, B. J. , Seow, C. Y. , and Pare, P. D. , 2001, “ Airway Narrowing Associated With Inhibition of Deep Inspiration During Methacholine Inhalation in Asthmatics,” Am. J. Respir. Crit. Care Med., 164(2), pp. 216–218. [CrossRef] [PubMed]
Tawhai, M. H. , Nash, M. P. , Lin, C. L. , and Hoffman, E. A. , 2009, “ Supine and Prone Differences in Regional Lung Density and Pleural Pressure Gradients in the Human Lung With Constant Shape,” J. Appl. Physiol., 107(3), pp. 912–920. [CrossRef] [PubMed]
Ballard, R. D. , Irvin, C. G. , Martin, R. J. , Pak, J. , Pandey, R. , and White, D. P. , 1990, “ Influence of Sleep on Lung Volume in Asthmatic Patients and Normal Subjects,” J. Appl. Physiol., 68(5), pp. 2034–2041. [CrossRef] [PubMed]
Pare, P. D. , 2003, “ Airway Hyperresponsiveness in Asthma: Geometry is Not Everything!,” Am. J. Respir. Crit. Care Med., 168(8), pp. 913–914. [CrossRef] [PubMed]
Sera, T. , Yokota, H. , Uesugi, K. , and Yagi, N. , 2013, “ Airway Distension During Lung Inflation in Healthy and Allergic-Sensitised Mice In Vivo,” Respir. Physiol. Neurobiol., 185(3), pp. 639–646. [CrossRef] [PubMed]
Brown, R. H. , Mitzner, W. , Bulut, Y. , and Wagner, E. M. , 1997, “ Effect of Lung Inflation In Vivo on Airways With Smooth Muscle Tone or Edema,” J. Appl. Physiol., 82(2), pp. 491–499. [CrossRef] [PubMed]
Pare, P. D. , and Mitzner, W. , 2012, “ Airway-Parenchymal Interdependence,” Compr. Physiol., 2(3), pp. 1921–1935. [PubMed]
Mauad, T. , Silva, L. F. , Santos, M. A. , Grinberg, L. , Bernardi, F. D. , Martins, M. A. , Saldiva, P. H. , and Dolhnikoff, M. , 2004, “ Abnormal Alveolar Attachments With Decreased Elastic Fiber Content in Distal Lung in Fatal Asthma,” Am. J. Respir. Crit. Care Med., 170(8), pp. 857–862. [CrossRef] [PubMed]
Pare, P. D. , and Bai, T. R. , 1995, “ The Consequences of Chronic Allergic Inflammation,” Thorax, 50(4), pp. 328–332. [CrossRef] [PubMed]
Verbeken, E. K. , Cauberghs, M. , Mertens, I. , Clement, J. , Lauweryns, J. M. , and Van de Woestijne, K. P. , 1992, “ The Senile Lung. Comparison With Normal and Emphysematous Lungs—1: Structural Aspects,” Chest, 101(3), pp. 793–799. [CrossRef] [PubMed]
Harris, R. S. , 1959, “ Tracheal Extension in Respiration,” Thorax, 14, pp. 201–210. [CrossRef] [PubMed]
Janssens, J. P. , Pache, J. C. , and Nicod, L. P. , 1999, “ Physiological Changes in Respiratory Function Associated With Ageing,” Eur. Respir. J., 13(1), pp. 197–205. [CrossRef] [PubMed]
Scichilone, N. , Marchese, R. , Catalano, F. , Togias, A. , Vignola, A. M. , and Bellia, V. , 2004, “ The Bronchodilatory Effect of Deep Inspiration Diminishes With Aging,” Respir. Med., 98(9), pp. 838–843. [CrossRef] [PubMed]
Hirota, N. , and Martin, J. G. , 2013, “ Mechanisms of Airway Remodeling,” Chest, 144(3), pp. 1026–1032. [CrossRef] [PubMed]
Kelly, V. J. , Brown, N. J. , Sands, S. A. , Borg, B. M. , King, G. G. , and Thompson, B. R. , 2012, “ Effect of Airway Smooth Muscle Tone on Airway Distensibility Measured by the Forced Oscillation Technique in Adults With Asthma,” J. Appl. Physiol., 112(9), pp. 1494–1503. [CrossRef] [PubMed]
Slats, A. M. , Janssen, K. , van Schadewijk, A. , van der Plas, D. T. , Schot, R. , van den Aardweg, J. G. , de Jongste, J. C. , Hiemstra, P. S. , Mauad, T. , Rabe, K. F. , and Sterk, P. J. , 2007, “ Bronchial Inflammation and Airway Responses to Deep Inspiration in Asthma and Chronic Obstructive Pulmonary Disease,” Am. J. Respir. Crit. Care Med., 176(2), pp. 121–128. [CrossRef] [PubMed]
Montaudon, M. , Lederlin, M. , Reich, S. , Begueret, H. , Tunon-de-Lara, J. M. , Marthan, R. , Berger, P. , and Laurent, F. , 2009, “ Bronchial Measurements in Patients With Asthma: Comparison of Quantitative Thin-Section CT Findings With Those in Healthy Subjects and Correlation With Pathologic Findings,” Radiology, 253(3), pp. 844–853. [CrossRef] [PubMed]
Farah, C. S. , Keulers, L. A. , Hardaker, K. M. , Peters, M. J. , Berend, N. , Postma, D. S. , Salome, C. M. , and King, G. G. , 2015, “ Association Between Peripheral Airway Function and Neutrophilic Inflammation in Asthma,” Respirology, 20(6), pp. 975–981. [CrossRef] [PubMed]
Gelb, A. F. , Licuanan, J. , Shinar, C. M. , and Zamel, N. , 2002, “ Unsuspected Loss of Lung Elastic Recoil in Chronic Persistent Asthma,” Chest, 121(3), pp. 715–721. [CrossRef] [PubMed]
Gelb, A. F. , and Zamel, N. , 2000, “ Unsuspected Pseudophysiologic Emphysema in Chronic Persistent Asthma,” Am. J. Respir. Crit. Care Med., 162(5), pp. 1778–1782. [CrossRef] [PubMed]
Allen, N. D. , Davis, B. E. , and Cockcroft, D. W. , 2008, “ Correlation Between Airway Inflammation and Loss of Deep-Inhalation Bronchoprotection in Asthma,” Ann. Allergy Asthma Immunol., 101(4), pp. 413–418. [CrossRef] [PubMed]
Fish, J. E. , Ankin, M. G. , Kelly, J. F. , and Peterman, V. I. , 1981, “ Regulation of Bronchomotor Tone by Lung Inflation in Asthmatic and Nonasthmatic Subjects,” J. Appl. Physiol., 50(5), pp. 1079–1086. [CrossRef]
Scichilone, N. , Permutt, S. , and Togias, A. , 2001, “ The Lack of the Bronchoprotective and Not the Bronchodilatory Ability of Deep Inspiration is Associated With Airway Hyperresponsiveness,” Am. J. Respir. Crit. Care Med., 163(2), pp. 413–419. [CrossRef] [PubMed]
Skloot, G. , Permutt, S. , and Togias, A. , 1995, “ Airway Hyperresponsiveness in Asthma: A Problem of Limited Smooth Muscle Relaxation With Inspiration,” J. Clin. Invest., 96(5), pp. 2393–2403. [CrossRef] [PubMed]
Burns, C. B. , Taylor, W. R. , and Ingram, R. H., Jr. , 1985, “ Effects of Deep Inhalation in Asthma: Relative Airway and Parenchymal Hysteresis,” J. Appl. Physiol., 59(5), pp. 1590–1596. [CrossRef] [PubMed]
Lim, T. K. , Pride, N. B. , and Ingram, R. H., Jr. , 1987, “ Effects of Volume History During Spontaneous and Acutely Induced Air-Flow Obstruction in Asthma,” Am. Rev. Respir. Dis., 135(3), pp. 591–596. https://www.atsjournals.org/doi/abs/10.1164/ajrccm/136.3.793a [PubMed]
Black, L. D. , Henderson, A. C. , Atileh, H. , Israel, E. , Ingenito, E. P. , and Lutchen, K. R. , 2004, “ Relating Maximum Airway Dilation and Subsequent Reconstriction to Reactivity in Human Lungs,” J. Appl. Physiol., 96(5), pp. 1808–1814. [CrossRef] [PubMed]
Wheatley, J. R. , Pare, P. D. , and Engel, L. A. , 1989, “ Reversibility of Induced Bronchoconstriction by Deep Inspiration in Asthmatic and Normal Subjects,” Eur. Respir. J., 2(4), pp. 331–339. https://www.ncbi.nlm.nih.gov/pubmed/2661258 [PubMed]
Scichilone, N. , Marchese, R. , Catalano, F. , Vignola, A. M. , Togias, A. , and Bellia, V. , 2004, “ Bronchodilatory Effect of Deep Inspiration is Absent in Subjects With Mild COPD,” Chest, 125(6), pp. 2029–2035. [CrossRef] [PubMed]
Mansell, A. , Dubrawsky, C. , Levison, H. , Bryan, A. C. , and Crozier, D. N. , 1974, “ Lung Elastic Recoil in Cystic Fibrosis,” Am. Rev. Respir. Dis., 109(2), pp. 190–197. [PubMed]
Nishino, M. , Siewert, B. , Roberts, D. H. , Gautam, S. , Boiselle, P. M. , Raptopoulos, V. , and Hatabu, H. , 2006, “ Excessive Collapsibility of Bronchi in Bronchiectasis: Evaluation on Volumetric Expiratory High-Resolution CT,” J. Comput. Assisted Tomogr., 30(3), pp. 474–478. [CrossRef]
Jones, R. L. , and Nzekwu, M. M. , 2006, “ The Effects of Body Mass Index on Lung Volumes,” Chest, 130(3), pp. 827–833. [CrossRef] [PubMed]
Holguin, F. , Cribbs, S. , Fitzpatrick, A. M. , Ingram , R. H., Jr. , and Jackson, A. C. , 2010, “ A Deep Breath Bronchoconstricts Obese Asthmatics,” J. Asthma, 47(1), pp. 55–60. [CrossRef] [PubMed]
Skloot, G. , Schechter, C. , Desai, A. , and Togias, A. , 2011, “ Impaired Response to Deep Inspiration in Obesity,” J. Appl. Physiol., 111(3), pp. 726–734. [CrossRef] [PubMed]
Boulet, L. P. , Turcotte, H. , Boulet, G. , Simard, B. , and Robichaud, P. , 2005, “ Deep Inspiration Avoidance and Airway Response to Methacholine: Influence of Body Mass Index,” Can. Respir. J., 12(7), pp. 371–376. [CrossRef] [PubMed]
Richmond, I. , Booth, H. , Ward, C. , and Walters, E. H. , 1996, “ Intrasubject Variability in Airway Inflammation in Biopsies in Mild to Moderate Stable Asthma,” Am. J. Respir. Crit. Care Med., 153(3), pp. 899–903. [CrossRef] [PubMed]
Pascoe, C. D. , Seow, C. Y. , Hackett, T. L. , Pare, P. D. , and Donovan, G. M. , 2017, “ Heterogeneity of Airway Wall Dimensions in Humans: A Critical Determinant of Lung Function in Asthmatics and Nonasthmatics,” Am. J. Physiol. Lung Cell Mol. Physiol., 312(3), pp. L425–L431. [CrossRef] [PubMed]
Lee-Gosselin, A. , Pascoe, C. D. , Couture, C. , Pare, P. D. , and Bosse, Y. , 2013, “ Does the Length Dependency of Airway Smooth Muscle Force Contribute to Airway Hyperresponsiveness?,” J. Appl. Physiol., 115(9), pp. 1304–1315. [CrossRef] [PubMed]
Bosse, Y. , 2012, “ Asthmatic Airway Hyperresponsiveness: The Ants in the Tree,” Trends Mol. Med., 18(11), pp. 627–633. [CrossRef] [PubMed]
Hasegawa, M. , Makita, H. , Nasuhara, Y. , Odajima, N. , Nagai, K. , Ito, Y. , Betsuyaku, T. , and Nishimura, M. , 2009, “ Relationship Between Improved Airflow Limitation and Changes in Airway Calibre Induced by Inhaled Anticholinergic Agents in COPD,” Thorax, 64(4), pp. 332–338. [CrossRef] [PubMed]
Brown, R. H. , Wizeman, W. , Danek, C. , and Mitzner, W. , 2005, “ Effect of Bronchial Thermoplasty on Airway Distensibility,” Eur. Respir. J., 26(2), pp. 277–282. [CrossRef] [PubMed]
Milanese, M. , Saporiti, R. , Bartolini, S. , Pellegrino, R. , Baroffio, M. , Brusasco, V. , and Crimi, E. , 2009, “ Bronchodilator Effects of Exercise Hyperpnea and Albuterol in Mild-to-Moderate Asthma,” J. Appl. Physiol., 107(2), pp. 494–499. [CrossRef] [PubMed]
Orehek, J. , Charpin, D. , Velardocchio, J. M. , and Grimaud, C. , 1980, “ Bronchomotor Effect of Bronchoconstriction-Induced Deep Inspirations in Asthmatics,” Am. Rev. Respir. Dis., 121(2), pp. 297–305. [PubMed]
LaPrad, A. S. , and Lutchen, K. R. , 2008, “ Respiratory Impedance Measurements for Assessment of Lung Mechanics: Focus on Asthma,” Respir. Physiol. Neurobiol., 163(1–3), pp. 64–73. [CrossRef] [PubMed]
Young, H. M. , Guo, F. , Eddy, R. L. , Maksym, G. , and Parraga, G. , 2018, “ Oscillometry and Pulmonary MRI Measurements of Ventilation Heterogeneity in Obstructive Lung Disease: Relationship to Quality of Life and Disease Control,” J. Appl. Physiol., 125(1), pp. 73–85. [CrossRef] [PubMed]
Hark, W. T. , Thompson, W. M. , McLaughlin, T. E. , Wheatley, L. M. , and Platts-Mills, T. A. , 2005, “ Spontaneous Sigh Rates During Sedentary Activity: Watching Television vs Reading,” Ann. Allergy Asthma Immunol., 94(2), pp. 247–250. [CrossRef] [PubMed]
Bendixen, H. H. , Smith, G. M. , and Mead, J. , 1964, “ Pattern of Ventilation in Young Adults,” J. Appl. Physiol., 19, pp. 195–198. [CrossRef] [PubMed]

Figures

Grahic Jump Location
Fig. 1

The changes in luminal geometry overestimate the stretch the ASM undergoes during a deep inspiration (DI). The schematic illustrates a normal (left) and an asthmatic (right) airways at FRC and after a DI to TLC. The dimensions are zoomed but at scale to an average airway of the ten generation. The springs represent lung recoil. They are stretched at TLC relative to FRC. The arrow at approximately 2 o'clock is the radius (in mm) of the airway lumen (rL). The arrow at approximately 1 o'clock is the radius up to the middle of the airway smooth muscle layer (rM). The material composing the airway wall was considered inextensible. Notice the thinning of the airway wall when the lungs are inflating to TLC. It this schematic it was assumed that the luminal geometry at FRC was equal between normal and asthmatic. It was further assumed that the DI was increasing luminal radius by 25% in both normal and asthmatic, so that the luminal geometry at TLC was also equal between normal and asthmatic. The schematic demonstrates that a 25% increase of luminal perimeter (PL) only causes a 21.2% increase of the perimeter at the middle of the ASM layer (PM). This effect is further amplified in asthmatic because of a thicker airway wall (25 versus 18.2%). The mathematics is developed in the middle. Other abbreviations: AAW—area of the airway wall from the lumen to the middle of the ASM layer, AL—luminal area, AM—area internal to the middle of the ASM layer, and %Δ—change in percentage.

Grahic Jump Location
Fig. 2

Imagine an airway cut open longitudinally and unfolded to form the rectangle on top (a). The letter a represents the airway perimeter and, in this example, is set to 10 mm. The letter b is the airway longitudinal distance covered by the ASM bundle going around the full circumference of the airway. Finally, the letter c represents the length of the ASM bundle and, in this example, is set at an angle 75 deg off the long axis of the airway. Using trigonometry, b and c can be determined. Now imagine that this airway is stretched radially to increase its perimeter by 25%. On the flattened airway shown in (a), this would increase the height of the rectangle by 25% without changing its length (b). Compared to (a), the length of a would increase by 25%, the length of b would remain unchanged and the length of c would increase by 23.5%. The angle of c would also change to 77.9 deg. Therefore, a radial stretch to the airway increasing its perimeter by 25% is expected to strain the ASM bundle by only 23.5%. Now imagine that the airway length is also strained by 25%. On the flattened airway shown in (b), this would increase the length of the rectangle by 25% (c). Compared to (a), the length of a, b, and c would all increase by 25%. In contrast to (b), the angle of c would remain unchanged. Therefore, when both radial and longitudinal strains are applied simultaneously at the same magnitude on an airway, the strain on the ASM is also of this magnitude.

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