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Monitoring airway mucus flow and ciliary activity with optical coherence tomographyAmy L. Oldenburg, Raghav K. Chhetri, David B. Hill, and Brian Button »View Author Affiliations
Amy L. Oldenburg,1,2,*
Raghav K. Chhetri,1
David B. Hill,3
and Brian Button3
1Department of Physics and Astronomy, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA 2Biomedical Research Imaging Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA 3Cystic Fibrosis/Pulmonary Research and Treatment Center, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA *Corresponding author: aold@physics.unc.edu |
Biomedical Optics Express, Vol. 3, Issue 9, pp. 1978-1992 (2012)
http://dx.doi.org/10.1364/BOE.3.001978
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Abstract
Muco-ciliary transport in the human airway is a crucial defense mechanism for removing inhaled pathogens. Optical coherence tomography (OCT) is well-suited to monitor functional dynamics of cilia and mucus on the airway epithelium. Here we demonstrate several OCT-based methods upon an actively transporting in vitro bronchial epithelial model and ex vivo mouse trachea. We show quantitative flow imaging of optically turbid mucus, semi-quantitative analysis of the ciliary beat frequency, and functional imaging of the periciliary layer. These may translate to clinical methods for endoscopic monitoring of muco-ciliary transport in diseases such as cystic fibrosis and chronic obstructive pulmonary disease (COPD).
© 2012 OSA
OCIS Codes
(110.6150) Imaging systems : Speckle imaging
(170.3880) Medical optics and biotechnology : Medical and biological imaging
(170.4500) Medical optics and biotechnology : Optical coherence tomography
(110.0113) Imaging systems : Imaging through turbid media
(170.2655) Medical optics and biotechnology : Functional monitoring and imaging
(110.4153) Imaging systems : Motion estimation and optical flow
ToC Category:
Optical Coherence Tomography
History
Original Manuscript: May 21, 2012
Revised Manuscript: July 6, 2012
Manuscript Accepted: July 6, 2012
Published: August 1, 2012
Citation
Amy L. Oldenburg, Raghav K. Chhetri, David B. Hill, and Brian Button, "Monitoring airway mucus flow and ciliary activity with optical coherence
tomography," Biomed. Opt. Express 3, 1978-1992 (2012)
http://www.opticsinfobase.org/boe/abstract.cfm?URI=boe-3-9-1978
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McWilliams, A.
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O’Brien, E. T.
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- J. C. Hogg, F. Chu, S. Utokaparch, R. Woods, W. M. Elliott, L. Buzatu, R. M. Cherniack, R. M. Rogers, F. C. Sciurba, H. O. Coxson, and P. D. Paré, “The nature of small-airway obstruction in chronic obstructive pulmonary disease,” N. Engl. J. Med.350(26), 2645–2653 (2004). [CrossRef] [PubMed]
- H. O. Coxson, B. Quiney, D. D. Sin, L. Xing, A. M. McWilliams, J. R. Mayo, and S. Lam, “Airway wall thickness assessed using computed tomography and optical coherence tomography,” Am. J. Respir. Crit. Care Med.177(11), 1201–1206 (2008). [CrossRef] [PubMed]
- L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med.17(8), 1010–1014 (2011). [CrossRef] [PubMed]
- S. Lam, B. Standish, C. Baldwin, A. McWilliams, J. leRiche, A. Gazdar, A. I. Vitkin, V. Yang, N. Ikeda, and C. MacAulay, “In vivo optical coherence tomography imaging of preinvasive bronchial lesions,” Clin. Cancer Res.14(7), 2006–2011 (2008). [CrossRef] [PubMed]
- M. L. Fulcher, S. Gabriel, K. A. Burns, J. R. Yankaskas, and S. H. Randell, “Well-differentiated human airway epithelial cell cultures,” Methods Mol. Med.107, 183–206 (2005). [PubMed]
- J. Su, J. Zhang, L. Yu, H. G Colt, M. Brenner, and Z. Chen, “Real-time swept source optical coherence tomography imaging of the human airway using a microelectromechanical system endoscope and digital signal processor,” J. Biomed. Opt.13(3), 030506 (2008). [CrossRef] [PubMed]
- E. Puchelle, J. M. Zahm, and D. Quemada, “Rheological properties controlling mucociliary frequency and respiratory mucus transport,” Biorheology24(6), 557–563 (1987). [PubMed]
- S. H. Donaldson, W. D. Bennett, K. L. Zeman, M. R. Knowles, R. Tarran, and R. C. Boucher, “Mucus clearance and lung function in cystic fibrosis with hypertonic saline,” N. Engl. J. Med.354(3), 241–250 (2006). [CrossRef] [PubMed]
- J. Su, J. Zhang, L. Yu, H. G Colt, M. Brenner, and Z. Chen, “Real-time swept source optical coherence tomography imaging of the human airway using a microelectromechanical system endoscope and digital signal processor,” J. Biomed. Opt.13(3), 030506 (2008). [CrossRef] [PubMed]
AJR Am. J. Roentgenol.
- R. M. Shah, W. Sexauer, B. J. Ostrum, S. B. Fiel, and A. C. Friedman, “High-resolution CT in the acute exacerbation of cystic fibrosis: evaluation of acute findings, reversibility of those findings, and clinical correlation,” AJR Am. J. Roentgenol.169(2), 375–380 (1997). [PubMed]
Am. J. Respir. Crit. Care Med.
- C. Pitris, M. E. Brezinski, B. E. Bouma, G. J. Tearney, J. F. Southern, and J. G. Fujimoto, “High resolution imaging of the upper respiratory tract with optical coherence tomography: a feasibility study,” Am. J. Respir. Crit. Care Med.157(5 Pt 1), 1640–1644 (1998). [PubMed]
Am. J. Physiol.
- A. B. Lansley, M. J. Sanderson, and E. R. Dirksen, “Control of the beat cycle of respiratory tract cilia by Ca2+ and cAMP,” Am. J. Physiol.263(2 Pt 1), L232–L242 (1992). [PubMed]
Am. J. Respir. Crit. Care Med.
- H. O. Coxson, B. Quiney, D. D. Sin, L. Xing, A. M. McWilliams, J. R. Mayo, and S. Lam, “Airway wall thickness assessed using computed tomography and optical coherence tomography,” Am. J. Respir. Crit. Care Med.177(11), 1201–1206 (2008). [CrossRef] [PubMed]
Am. J. Respir. Crit. Care Med.
- J. A. Regnis, M. Robinson, D. L. Bailey, P. Cook, P. Hooper, H. K. Chan, I. Gonda, G. Bautovich, and P. T. Bye, “Mucociliary clearance in patients with cystic fibrosis and in normal subjects,” Am. J. Respir. Crit. Care Med.150(1), 66–71 (1994). [PubMed]
Am. J. Respir. Crit. Care Med.
- A. Wanner, M. Salathé, and T. G. O’Riordan, “Mucociliary clearance in the airways,” Am. J. Respir. Crit. Care Med.154(6 Pt 1), 1868–1902 (1996). [PubMed]
- J. P. Williamson, R. A. McLaughlin, W. J. Noffsinger, A. L. James, V. A. Baker, A. Curatolo, J. J. Armstrong, A. Regli, K. L. Shepherd, G. B. Marks, D. D. Sampson, D. R. Hillman, and P. R. Eastwood, “Elastic properties of the central airways in obstructive lung diseases measured using anatomical optical coherence tomography,” Am. J. Respir. Crit. Care Med.183(5), 612–619 (2011). [CrossRef] [PubMed]
Anesth. Analg.
- B. R. Manawadu, S. R. Mostow, and F. M. LaForce, “Impairment of tracheal ring ciliary activity by halothane,” Anesth. Analg.58(6), 500–504 (1979). [CrossRef] [PubMed]
Appl. Opt.
- D. L. Marks, A. L. Oldenburg, J. J. Reynolds, and S. A. Boppart, “Digital algorithm for dispersion correction in optical coherence tomography for homogeneous and stratified media,” Appl. Opt.42(2), 204–217 (2003). [CrossRef] [PubMed]
Biomed. Opt. Express
- V. J. Srinivasan, H. Radhakrishnan, E. H. Lo, E. T. Mandeville, J. Y. Jiang, S. Barry, and A. E. Cable, “OCT methods for capillary velocimetry,” Biomed. Opt. Express3(3), 612–629 (2012). [CrossRef] [PubMed]
- S. Jonas, D. Bhattacharya, M. K. Khokha, and M. A. Choma, “Microfluidic characterization of cilia-driven fluid flow using optical coherence tomography-based particle tracking velocimetry,” Biomed. Opt. Express2(7), 2022–2034 (2011). [CrossRef] [PubMed]
Biophys. J.
- A. L. Oldenburg, C. M. Gallippi, F. Tsui, T. C. Nichols, K. N. Beicker, R. K. Chhetri, D. Spivak, A. Richardson, and T. H. Fischer, “Magnetic and contrast properties of labeled platelets for magnetomotive optical coherence tomography,” Biophys. J.99(7), 2374–2383 (2010). [CrossRef] [PubMed]
Biophys. J.
- D. B. Hill, V. Swaminathan, A. Estes, J. Cribb, E. T. O’Brien, C. W. Davis, and R. Superfine, “Force generation and dynamics of individual cilia under external loading,” Biophys. J.98(1), 57–66 (2010). [CrossRef] [PubMed]
Biorheology
- E. Puchelle, J. M. Zahm, and D. Quemada, “Rheological properties controlling mucociliary frequency and respiratory mucus transport,” Biorheology24(6), 557–563 (1987). [PubMed]
Br. J. Anaesth.
- J. H. Raphael, D. A. Selwyn, S. D. Mottram, J. A. Langton, and C. O’Callaghan, “Effects of 3 MAC of halothane, enflurane and isoflurane on cilia beat frequency of human nasal epithelium in vitro,” Br. J. Anaesth.76(1), 116–121 (1996). [CrossRef] [PubMed]
Cell
- H. Matsui, B. R. Grubb, R. Tarran, S. H. Randell, J. T. Gatzy, C. W. Davis, and R. C. Boucher, “Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease,” Cell95(7), 1005–1015 (1998). [CrossRef] [PubMed]
Chest
- T. Aikawa, S. Shimura, H. Sasaki, M. Ebina, and T. Takishima, “Marked goblet cell hyperplasia with mucus accumulation in the airways of patients who died of severe acute asthma attack,” Chest101(4), 916–921 (1992). [CrossRef] [PubMed]
- R. G. Michel, G. T. Kinasewitz, K. M. Fung, and J. I. Keddissi, “Optical coherence tomography as an adjunct to flexible bronchoscopy in the diagnosis of lung cancer: a pilot study,” Chest138(4), 984–988 (2010). [CrossRef] [PubMed]
- G. C. Smaldone, W. M. Foster, T. G. O’Riordan, M. S. Messina, R. J. Perry, and E. G. Langenback, “Regional impairment of mucociliary clearance in chronic obstructive pulmonary disease,” Chest103(5), 1390–1396 (1993). [CrossRef] [PubMed]
Clin. Cancer Res.
- S. Lam, B. Standish, C. Baldwin, A. McWilliams, J. leRiche, A. Gazdar, A. I. Vitkin, V. Yang, N. Ikeda, and C. MacAulay, “In vivo optical coherence tomography imaging of preinvasive bronchial lesions,” Clin. Cancer Res.14(7), 2006–2011 (2008). [CrossRef] [PubMed]
Clin. Otolaryngol. Allied Sci.
- A. Robertson, W. Stannard, C. Passant, C. O’Callaghan, and A. Banerjee, “What effect does isoflurane have upon ciliary beat pattern: an in vivo study,” Clin. Otolaryngol. Allied Sci.29(2), 157–160 (2004). [CrossRef] [PubMed]
Curr. Opin. Allergy Clin. Immunol.
- M. B. Antunes and N. A. Cohen, “Mucociliary clearance--a critical upper airway host defense mechanism and methods of assessment,” Curr. Opin. Allergy Clin. Immunol.7(1), 5–10 (2007). [CrossRef] [PubMed]
IEEE Trans. Ultrason. Ferroelectr. Freq. Control
- I. A. Hein and W. R. O’Brien, “Current time-domain methods for assessing tissue motion by analysis from reflected ultrasound echoes-a review,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control40(2), 84–102 (1993). [CrossRef] [PubMed]
IEEE Trans. Biomed. Eng.
- L. N. Bohs and G. E. Trahey, “A novel method for angle independent ultrasonic imaging of blood flow and tissue motion,” IEEE Trans. Biomed. Eng.38(3), 280–286 (1991). [CrossRef] [PubMed]
J. Appl. Physiol.
- W. M. Foster, E. Langenback, and E. H. Bergofsky, “Measurement of tracheal and bronchial mucus velocities in man: relation to lung clearance,” J. Appl. Physiol.48(6), 965–971 (1980). [PubMed]
J. Biomed. Opt.
- J. Su, J. Zhang, L. Yu, H. G Colt, M. Brenner, and Z. Chen, “Real-time swept source optical coherence tomography imaging of the human airway using a microelectromechanical system endoscope and digital signal processor,” J. Biomed. Opt.13(3), 030506 (2008). [CrossRef] [PubMed]
- K. Jeong, J. J. Turek, and D. D. Nolte, “Speckle fluctuation spectroscopy of intracellular motion in living tissue using coherence-domain digital holography,” J. Biomed. Opt.15(3), 030514 (2010). [CrossRef] [PubMed]
- D. D. Nolte, R. An, J. Turek, and K. Jeong, “Holographic tissue dynamics spectroscopy,” J. Biomed. Opt.16(8), 087004 (2011). [CrossRef] [PubMed]
J. Clin. Invest.
- M. R. Knowles and R. C. Boucher, “Mucus clearance as a primary innate defense mechanism for mammalian airways,” J. Clin. Invest.109(5), 571–577 (2002). [PubMed]
- H. Matsui, S. H. Randell, S. W. Peretti, C. W. Davis, and R. C. Boucher, “Coordinated clearance of periciliary liquid and mucus from airway surfaces,” J. Clin. Invest.102(6), 1125–1131 (1998). [CrossRef] [PubMed]
Laser Phys. Lett.
- Z. Y. Shen, M. Wang, Y. H. Ji, Y. H. He, X. S. Dai, P. Li, and H. Ma, “Transverse flow velocity quantification using optical coherence tomography with correlation,” Laser Phys. Lett.8(4), 318–323 (2011). [CrossRef]
Methods Mol. Med.
- M. L. Fulcher, S. Gabriel, K. A. Burns, J. R. Yankaskas, and S. H. Randell, “Well-differentiated human airway epithelial cell cultures,” Methods Mol. Med.107, 183–206 (2005). [PubMed]
N. Engl. J. Med.
- J. C. Hogg, F. Chu, S. Utokaparch, R. Woods, W. M. Elliott, L. Buzatu, R. M. Cherniack, R. M. Rogers, F. C. Sciurba, H. O. Coxson, and P. D. Paré, “The nature of small-airway obstruction in chronic obstructive pulmonary disease,” N. Engl. J. Med.350(26), 2645–2653 (2004). [CrossRef] [PubMed]
- S. H. Donaldson, W. D. Bennett, K. L. Zeman, M. R. Knowles, R. Tarran, and R. C. Boucher, “Mucus clearance and lung function in cystic fibrosis with hypertonic saline,” N. Engl. J. Med.354(3), 241–250 (2006). [CrossRef] [PubMed]
Nat. Med.
- L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med.17(8), 1010–1014 (2011). [CrossRef] [PubMed]
Opt. Express
- A. L. Oldenburg, V. Crecea, S. A. Rinne, and S. A. Boppart, “Phase-resolved magnetomotive OCT for imaging nanomolar concentrations of magnetic nanoparticles in tissues,” Opt. Express16(15), 11525–11539 (2008). [PubMed]
Opt. Express
- B. White, M. Pierce, N. Nassif, B. Cense, B. Park, G. Tearney, B. Bouma, T. Chen, and J. de Boer, “In vivo dynamic human retinal blood flow imaging using ultra-high-speed spectral domain optical coherence tomography,” Opt. Express11(25), 3490–3497 (2003). [CrossRef] [PubMed]
- J. Schmitt, “OCT elastography: imaging microscopic deformation and strain of tissue,” Opt. Express3(6), 199–211 (1998). [CrossRef] [PubMed]
- G. Liu, L. Chou, W. Jia, W. Qi, B. Choi, and Z. Chen, “Intensity-based modified Doppler variance algorithm: application to phase instable and phase stable optical coherence tomography systems,” Opt. Express19(12), 11429–11440 (2011). [CrossRef] [PubMed]
Opt. Lett.
- Y. Wang and R. Wang, “Autocorrelation optical coherence tomography for mapping transverse particle-flow velocity,” Opt. Lett.35(21), 3538–3540 (2010). [CrossRef] [PubMed]
- E. A. Swanson, J. A. Izatt, M. R. Hee, D. Huang, C. P. Lin, J. S. Schuman, C. A. Puliafito, and J. G. Fujimoto, “In vivo retinal imaging by optical coherence tomography,” Opt. Lett.18(21), 1864–1866 (1993). [CrossRef] [PubMed]
- Y. Zhao, Z. Chen, C. Saxer, Q. Shen, S. Xiang, J. F. de Boer, and J. S. Nelson, “Doppler standard deviation imaging for clinical monitoring of in vivo human skin blood flow,” Opt. Lett.25(18), 1358–1360 (2000). [CrossRef] [PubMed]
- J. A. Izatt, M. D. Kulkarni, S. Yazdanfar, J. K. Barton, and A. J. Welch, “In vivo bidirectional color Doppler flow imaging of picoliter blood volumes using optical coherence tomography,” Opt. Lett.22(18), 1439–1441 (1997). [CrossRef] [PubMed]
- B. Povazay, K. Bizheva, A. Unterhuber, B. Hermann, H. Sattmann, A. F. Fercher, W. Drexler, A. Apolonski, W. J. Wadsworth, J. C. Knight, P. S. J. Russell, M. Vetterlein, and E. Scherzer, “Submicrometer axial resolution optical coherence tomography,” Opt. Lett.27(20), 1800–1802 (2002). [CrossRef] [PubMed]
Proc. Natl. Acad. Sci. U.S.A.
- S. Gueron, K. Levit-Gurevich, N. Liron, and J. J. Blum, “Cilia internal mechanism and metachronal coordination as the result of hydrodynamical coupling,” Proc. Natl. Acad. Sci. U.S.A.94(12), 6001–6006 (1997). [CrossRef] [PubMed]
Proc. SPIE
- A. L. Oldenburg and R. K. Chhetri, “Digital dispersion compensation for ultrabroad-bandwidth single-camera spectral-domain polarization-sensitive OCT,” Proc. SPIE7889, 78891V (2011).
2012, Srinivasan, Biomed. Opt. Express
- L. Liu, J. A. Gardecki, S. K. Nadkarni, J. D. Toussaint, Y. Yagi, B. E. Bouma, and G. J. Tearney, “Imaging the subcellular structure of human coronary atherosclerosis using micro-optical coherence tomography,” Nat. Med.17(8), 1010–1014 (2011). [CrossRef] [PubMed]
- A. L. Oldenburg and R. K. Chhetri, “Digital dispersion compensation for ultrabroad-bandwidth single-camera spectral-domain polarization-sensitive OCT,” Proc. SPIE7889, 78891V (2011).
- J. P. Williamson, R. A. McLaughlin, W. J. Noffsinger, A. L. James, V. A. Baker, A. Curatolo, J. J. Armstrong, A. Regli, K. L. Shepherd, G. B. Marks, D. D. Sampson, D. R. Hillman, and P. R. Eastwood, “Elastic properties of the central airways in obstructive lung diseases measured using anatomical optical coherence tomography,” Am. J. Respir. Crit. Care Med.183(5), 612–619 (2011). [CrossRef] [PubMed]
- D. D. Nolte, R. An, J. Turek, and K. Jeong, “Holographic tissue dynamics spectroscopy,” J. Biomed. Opt.16(8), 087004 (2011). [CrossRef] [PubMed]
- Z. Y. Shen, M. Wang, Y. H. Ji, Y. H. He, X. S. Dai, P. Li, and H. Ma, “Transverse flow velocity quantification using optical coherence tomography with correlation,” Laser Phys. Lett.8(4), 318–323 (2011). [CrossRef]
- D. B. Hill, V. Swaminathan, A. Estes, J. Cribb, E. T. O’Brien, C. W. Davis, and R. Superfine, “Force generation and dynamics of individual cilia under external loading,” Biophys. J.98(1), 57–66 (2010). [CrossRef] [PubMed]
- R. G. Michel, G. T. Kinasewitz, K. M. Fung, and J. I. Keddissi, “Optical coherence tomography as an adjunct to flexible bronchoscopy in the diagnosis of lung cancer: a pilot study,” Chest138(4), 984–988 (2010). [CrossRef] [PubMed]
- K. Jeong, J. J. Turek, and D. D. Nolte, “Speckle fluctuation spectroscopy of intracellular motion in living tissue using coherence-domain digital holography,” J. Biomed. Opt.15(3), 030514 (2010). [CrossRef] [PubMed]
- A. L. Oldenburg, C. M. Gallippi, F. Tsui, T. C. Nichols, K. N. Beicker, R. K. Chhetri, D. Spivak, A. Richardson, and T. H. Fischer, “Magnetic and contrast properties of labeled platelets for magnetomotive optical coherence tomography,” Biophys. J.99(7), 2374–2383 (2010). [CrossRef] [PubMed]
- A. L. Oldenburg, V. Crecea, S. A. Rinne, and S. A. Boppart, “Phase-resolved magnetomotive OCT for imaging nanomolar concentrations of magnetic nanoparticles in tissues,” Opt. Express16(15), 11525–11539 (2008). [PubMed]
- J. Su, J. Zhang, L. Yu, H. G Colt, M. Brenner, and Z. Chen, “Real-time swept source optical coherence tomography imaging of the human airway using a microelectromechanical system endoscope and digital signal processor,” J. Biomed. Opt.13(3), 030506 (2008). [CrossRef] [PubMed]
- H. O. Coxson, B. Quiney, D. D. Sin, L. Xing, A. M. McWilliams, J. R. Mayo, and S. Lam, “Airway wall thickness assessed using computed tomography and optical coherence tomography,” Am. J. Respir. Crit. Care Med.177(11), 1201–1206 (2008). [CrossRef] [PubMed]
- S. Lam, B. Standish, C. Baldwin, A. McWilliams, J. leRiche, A. Gazdar, A. I. Vitkin, V. Yang, N. Ikeda, and C. MacAulay, “In vivo optical coherence tomography imaging of preinvasive bronchial lesions,” Clin. Cancer Res.14(7), 2006–2011 (2008). [CrossRef] [PubMed]
- M. B. Antunes and N. A. Cohen, “Mucociliary clearance--a critical upper airway host defense mechanism and methods of assessment,” Curr. Opin. Allergy Clin. Immunol.7(1), 5–10 (2007). [CrossRef] [PubMed]
- S. H. Donaldson, W. D. Bennett, K. L. Zeman, M. R. Knowles, R. Tarran, and R. C. Boucher, “Mucus clearance and lung function in cystic fibrosis with hypertonic saline,” N. Engl. J. Med.354(3), 241–250 (2006). [CrossRef] [PubMed]
- M. L. Fulcher, S. Gabriel, K. A. Burns, J. R. Yankaskas, and S. H. Randell, “Well-differentiated human airway epithelial cell cultures,” Methods Mol. Med.107, 183–206 (2005). [PubMed]
- J. C. Hogg, F. Chu, S. Utokaparch, R. Woods, W. M. Elliott, L. Buzatu, R. M. Cherniack, R. M. Rogers, F. C. Sciurba, H. O. Coxson, and P. D. Paré, “The nature of small-airway obstruction in chronic obstructive pulmonary disease,” N. Engl. J. Med.350(26), 2645–2653 (2004). [CrossRef] [PubMed]
- A. Robertson, W. Stannard, C. Passant, C. O’Callaghan, and A. Banerjee, “What effect does isoflurane have upon ciliary beat pattern: an in vivo study,” Clin. Otolaryngol. Allied Sci.29(2), 157–160 (2004). [CrossRef] [PubMed]
- B. Povazay, K. Bizheva, A. Unterhuber, B. Hermann, H. Sattmann, A. F. Fercher, W. Drexler, A. Apolonski, W. J. Wadsworth, J. C. Knight, P. S. J. Russell, M. Vetterlein, and E. Scherzer, “Submicrometer axial resolution optical coherence tomography,” Opt. Lett.27(20), 1800–1802 (2002). [CrossRef] [PubMed]
- M. R. Knowles and R. C. Boucher, “Mucus clearance as a primary innate defense mechanism for mammalian airways,” J. Clin. Invest.109(5), 571–577 (2002). [PubMed]
- H. Matsui, S. H. Randell, S. W. Peretti, C. W. Davis, and R. C. Boucher, “Coordinated clearance of periciliary liquid and mucus from airway surfaces,” J. Clin. Invest.102(6), 1125–1131 (1998). [CrossRef] [PubMed]
- C. Pitris, M. E. Brezinski, B. E. Bouma, G. J. Tearney, J. F. Southern, and J. G. Fujimoto, “High resolution imaging of the upper respiratory tract with optical coherence tomography: a feasibility study,” Am. J. Respir. Crit. Care Med.157(5 Pt 1), 1640–1644 (1998). [PubMed]
- H. Matsui, B. R. Grubb, R. Tarran, S. H. Randell, J. T. Gatzy, C. W. Davis, and R. C. Boucher, “Evidence for periciliary liquid layer depletion, not abnormal ion composition, in the pathogenesis of cystic fibrosis airways disease,” Cell95(7), 1005–1015 (1998). [CrossRef] [PubMed]
- S. Gueron, K. Levit-Gurevich, N. Liron, and J. J. Blum, “Cilia internal mechanism and metachronal coordination as the result of hydrodynamical coupling,” Proc. Natl. Acad. Sci. U.S.A.94(12), 6001–6006 (1997). [CrossRef] [PubMed]
- R. M. Shah, W. Sexauer, B. J. Ostrum, S. B. Fiel, and A. C. Friedman, “High-resolution CT in the acute exacerbation of cystic fibrosis: evaluation of acute findings, reversibility of those findings, and clinical correlation,” AJR Am. J. Roentgenol.169(2), 375–380 (1997). [PubMed]
- A. Wanner, M. Salathé, and T. G. O’Riordan, “Mucociliary clearance in the airways,” Am. J. Respir. Crit. Care Med.154(6 Pt 1), 1868–1902 (1996). [PubMed]
- J. H. Raphael, D. A. Selwyn, S. D. Mottram, J. A. Langton, and C. O’Callaghan, “Effects of 3 MAC of halothane, enflurane and isoflurane on cilia beat frequency of human nasal epithelium in vitro,” Br. J. Anaesth.76(1), 116–121 (1996). [CrossRef] [PubMed]
- J. A. Regnis, M. Robinson, D. L. Bailey, P. Cook, P. Hooper, H. K. Chan, I. Gonda, G. Bautovich, and P. T. Bye, “Mucociliary clearance in patients with cystic fibrosis and in normal subjects,” Am. J. Respir. Crit. Care Med.150(1), 66–71 (1994). [PubMed]
- G. C. Smaldone, W. M. Foster, T. G. O’Riordan, M. S. Messina, R. J. Perry, and E. G. Langenback, “Regional impairment of mucociliary clearance in chronic obstructive pulmonary disease,” Chest103(5), 1390–1396 (1993). [CrossRef] [PubMed]
- I. A. Hein and W. R. O’Brien, “Current time-domain methods for assessing tissue motion by analysis from reflected ultrasound echoes-a review,” IEEE Trans. Ultrason. Ferroelectr. Freq. Control40(2), 84–102 (1993). [CrossRef] [PubMed]
- T. Aikawa, S. Shimura, H. Sasaki, M. Ebina, and T. Takishima, “Marked goblet cell hyperplasia with mucus accumulation in the airways of patients who died of severe acute asthma attack,” Chest101(4), 916–921 (1992). [CrossRef] [PubMed]
- A. B. Lansley, M. J. Sanderson, and E. R. Dirksen, “Control of the beat cycle of respiratory tract cilia by Ca2+ and cAMP,” Am. J. Physiol.263(2 Pt 1), L232–L242 (1992). [PubMed]
- L. N. Bohs and G. E. Trahey, “A novel method for angle independent ultrasonic imaging of blood flow and tissue motion,” IEEE Trans. Biomed. Eng.38(3), 280–286 (1991). [CrossRef] [PubMed]
- E. Puchelle, J. M. Zahm, and D. Quemada, “Rheological properties controlling mucociliary frequency and respiratory mucus transport,” Biorheology24(6), 557–563 (1987). [PubMed]
- W. M. Foster, E. Langenback, and E. H. Bergofsky, “Measurement of tracheal and bronchial mucus velocities in man: relation to lung clearance,” J. Appl. Physiol.48(6), 965–971 (1980). [PubMed]
- B. R. Manawadu, S. R. Mostow, and F. M. LaForce, “Impairment of tracheal ring ciliary activity by halothane,” Anesth. Analg.58(6), 500–504 (1979). [CrossRef] [PubMed]
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