Abstract

Motile cilia perform a range of important mechanosensory and chemosensory functions, along with expulsion of mucus and inhaled pathogens from the lungs. Here we demonstrate that spectral domain optical coherence phase microscopy (SD-OCPM), which combines the principles of optical coherence tomography (OCT) and confocal microscopy, is particularly well-suited for characterization of both morphology and the ciliary dynamics of mouse trachea. We present micro-anatomical images of mouse trachea, where different cell types can be clearly visualized. The phase contrast, which measures the sub-nanometer changes in axial optical pathlength is used to determine the frequency and direction of cilia beatings.

© 2015 Optical Society of America

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References

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2014 (3)

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

S. Bermbach, K. Weinhold, T. Roeder, F. Petersen, C. Kugler, T. Goldmann, J. Rupp, and P. König, “Mechanisms of cilia-driven transport in the airways in the absence of mucus,” Am. J. Respir. Cell. Mol. Biol. 51(1), 56–67 (2014).
[Crossref] [PubMed]

R. Ansari, C. Myrtus, R. Aherrahrou, J. Erdmann, A. Schweikard, and G. Hüttmann, “Ultrahigh-resolution, high-speed spectral domain optical coherence phase microscopy,” Opt. Lett. 39(1), 45–47 (2014).
[Crossref]

2013 (2)

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

P. O. Bagnaninchi, C. Holmes, and M. Tabrizian, “Monitoring cells in engineered tissues with optical coherence phase microscopy: Optical phase fluctuations as endogenous sources of contrast,” Proc. SPIE 8580, 85800E (2013).

2012 (2)

I. Shock, A. Barbul, P. Girshovitz, U. Nevo, R. Korenstein, and N. T. Shakeda, “Optical phase nanoscopy in red blood cells using low-coherence spectroscopy,” J. Biomed. Opt. 17(10), 101509 (2012).
[Crossref] [PubMed]

A. L. Oldenburg, R. K. Chhetri, D. B. Hill, and B. Button, “Monitoring airway mucus flow and ciliary activity with optical coherence tomography,” Biomed. Opt. Express 3(9), 1978–1992 (2012).
[Crossref] [PubMed]

2011 (2)

2009 (3)

C. Joo, E. Özkumurc, M. S. Ünlüc, and J. F. de Boer, “Spectral-domain optical coherence phase microscopy for labelfree multiplexed protein microarray assay,” Biosens. and Bioelectron. 25(2), 275–281 (2009).
[Crossref]

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

A. S. Shah, Y. Ben-Shahar, T. O. Moninger, J. N. Kline, and M. J. Welsh, “Motile cilia of human airway epithelia are chemosensory,” Science 325(5944), 1131–1134 (2009).
[Crossref] [PubMed]

2008 (2)

2006 (3)

P. Delmotte and M. J. Sanderson, “Ciliary beat frequency is maintained at a maximal rate in the small airways of mouse lung slices,” Am. J. Respir. Cell. Mol. Biol. 35(1), 110–117 (2006).
[Crossref] [PubMed]

B. W. Bisgrove and H. J. Yos, “The roles of cilia in developmental disorders and disease,” Development 133(21), 4131–4143 (2006).
[Crossref] [PubMed]

M. A. Choma, A. K. Ellerbee, S. Yazdanfar, and J. A. Izatt, “Doppler flow imaging of cytoplasmic streaming using spectral domain phase microscopy,” J. Biomed. Opt. 11(2), 024014 (2006).
[Crossref] [PubMed]

2005 (2)

1998 (1)

A. M. Lale, J. D. T. Mason, and N. S. Jones, “Mucociliary transport and its assessment: a review,” Clin. Otolaryng. Allied Sci. 23(5), 388–396 (1998).
[Crossref]

1994 (1)

1988 (1)

M. A. Sleigh, J. R. Blake, and N. Liron, “The propulsion of mucus by cilia,” Am. Rev. Respir. Dis. 137(3), 726–741 (1988).
[Crossref] [PubMed]

Aherrahrou, R.

Akkin, T.

Ansari, R.

Bagnaninchi, P. O.

P. O. Bagnaninchi, C. Holmes, and M. Tabrizian, “Monitoring cells in engineered tissues with optical coherence phase microscopy: Optical phase fluctuations as endogenous sources of contrast,” Proc. SPIE 8580, 85800E (2013).

Barbul, A.

I. Shock, A. Barbul, P. Girshovitz, U. Nevo, R. Korenstein, and N. T. Shakeda, “Optical phase nanoscopy in red blood cells using low-coherence spectroscopy,” J. Biomed. Opt. 17(10), 101509 (2012).
[Crossref] [PubMed]

Ben-Shahar, Y.

A. S. Shah, Y. Ben-Shahar, T. O. Moninger, J. N. Kline, and M. J. Welsh, “Motile cilia of human airway epithelia are chemosensory,” Science 325(5944), 1131–1134 (2009).
[Crossref] [PubMed]

Berbari, N. F.

N. Sharma, N. F. Berbari, and B. K. Yoder, “Ciliary dysfunction in developmental abnormalities and diseases,” Curr. Top. Dev. Biol. 85, 371–427 (2008).

Bermbach, S.

S. Bermbach, K. Weinhold, T. Roeder, F. Petersen, C. Kugler, T. Goldmann, J. Rupp, and P. König, “Mechanisms of cilia-driven transport in the airways in the absence of mucus,” Am. J. Respir. Cell. Mol. Biol. 51(1), 56–67 (2014).
[Crossref] [PubMed]

Bhattacharya, D.

Birket, S. E.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Bisgrove, B. W.

B. W. Bisgrove and H. J. Yos, “The roles of cilia in developmental disorders and disease,” Development 133(21), 4131–4143 (2006).
[Crossref] [PubMed]

Blake, J. R.

M. A. Sleigh, J. R. Blake, and N. Liron, “The propulsion of mucus by cilia,” Am. Rev. Respir. Dis. 137(3), 726–741 (1988).
[Crossref] [PubMed]

Boer, J. F. de

C. Joo, E. Özkumurc, M. S. Ünlüc, and J. F. de Boer, “Spectral-domain optical coherence phase microscopy for labelfree multiplexed protein microarray assay,” Biosens. and Bioelectron. 25(2), 275–281 (2009).
[Crossref]

Button, B.

Byan-Parker, S.

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Cense, B.

Chhetri, R. K.

Choma, M. A.

Chu, K. K.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Creazzo, T. L.

de Boer, J. F.

Delmotte, P.

P. Delmotte and M. J. Sanderson, “Ciliary beat frequency is maintained at a maximal rate in the small airways of mouse lung slices,” Am. J. Respir. Cell. Mol. Biol. 35(1), 110–117 (2006).
[Crossref] [PubMed]

Diephuis, B. J.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Dierksen, G.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Ellerbee, A. K.

M. A. Choma, A. K. Ellerbee, S. Yazdanfar, and J. A. Izatt, “Doppler flow imaging of cytoplasmic streaming using spectral domain phase microscopy,” J. Biomed. Opt. 11(2), 024014 (2006).
[Crossref] [PubMed]

M. A. Choma, A. K. Ellerbee, C. Yang, T. L. Creazzo, and J. A. Izatt, “Spectral-domain phase microscopy,” Opt. Lett. 30(10), 1162–1164 (2005).
[Crossref] [PubMed]

Erdmann, J.

Faulhammer, P.

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

Fujimoto, J.

Girshovitz, P.

I. Shock, A. Barbul, P. Girshovitz, U. Nevo, R. Korenstein, and N. T. Shakeda, “Optical phase nanoscopy in red blood cells using low-coherence spectroscopy,” J. Biomed. Opt. 17(10), 101509 (2012).
[Crossref] [PubMed]

Goldmann, T.

S. Bermbach, K. Weinhold, T. Roeder, F. Petersen, C. Kugler, T. Goldmann, J. Rupp, and P. König, “Mechanisms of cilia-driven transport in the airways in the absence of mucus,” Am. J. Respir. Cell. Mol. Biol. 51(1), 56–67 (2014).
[Crossref] [PubMed]

Grizzle, W. E.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Haberberger, R. V.

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

Hanes, J.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

Hartmann, P.

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

Hee, M.

Hill, D. B.

Holmes, C.

P. O. Bagnaninchi, C. Holmes, and M. Tabrizian, “Monitoring cells in engineered tissues with optical coherence phase microscopy: Optical phase fluctuations as endogenous sources of contrast,” Proc. SPIE 8580, 85800E (2013).

Houser, G. H.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Hüttmann, G.

Izatt, J.

Izatt, J. A.

M. A. Choma, A. K. Ellerbee, S. Yazdanfar, and J. A. Izatt, “Doppler flow imaging of cytoplasmic streaming using spectral domain phase microscopy,” J. Biomed. Opt. 11(2), 024014 (2006).
[Crossref] [PubMed]

M. A. Choma, A. K. Ellerbee, C. Yang, T. L. Creazzo, and J. A. Izatt, “Spectral-domain phase microscopy,” Opt. Lett. 30(10), 1162–1164 (2005).
[Crossref] [PubMed]

Jonas, S.

Jones, N. S.

A. M. Lale, J. D. T. Mason, and N. S. Jones, “Mucociliary transport and its assessment: a review,” Clin. Otolaryng. Allied Sci. 23(5), 388–396 (1998).
[Crossref]

Joo, C.

Khokha, M. K.

Klein, M. K.

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

Kline, J. N.

A. S. Shah, Y. Ben-Shahar, T. O. Moninger, J. N. Kline, and M. J. Welsh, “Motile cilia of human airway epithelia are chemosensory,” Science 325(5944), 1131–1134 (2009).
[Crossref] [PubMed]

König, P.

S. Bermbach, K. Weinhold, T. Roeder, F. Petersen, C. Kugler, T. Goldmann, J. Rupp, and P. König, “Mechanisms of cilia-driven transport in the airways in the absence of mucus,” Am. J. Respir. Cell. Mol. Biol. 51(1), 56–67 (2014).
[Crossref] [PubMed]

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

Korenstein, R.

I. Shock, A. Barbul, P. Girshovitz, U. Nevo, R. Korenstein, and N. T. Shakeda, “Optical phase nanoscopy in red blood cells using low-coherence spectroscopy,” J. Biomed. Opt. 17(10), 101509 (2012).
[Crossref] [PubMed]

Krain, B.

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

Kugler, C.

S. Bermbach, K. Weinhold, T. Roeder, F. Petersen, C. Kugler, T. Goldmann, J. Rupp, and P. König, “Mechanisms of cilia-driven transport in the airways in the absence of mucus,” Am. J. Respir. Cell. Mol. Biol. 51(1), 56–67 (2014).
[Crossref] [PubMed]

Kummer, W.

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

Lale, A. M.

A. M. Lale, J. D. T. Mason, and N. S. Jones, “Mucociliary transport and its assessment: a review,” Clin. Otolaryng. Allied Sci. 23(5), 388–396 (1998).
[Crossref]

Li, Y.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Lips, K. S.

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

Liron, N.

M. A. Sleigh, J. R. Blake, and N. Liron, “The propulsion of mucus by cilia,” Am. Rev. Respir. Dis. 137(3), 726–741 (1988).
[Crossref] [PubMed]

Liu, L.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Mason, J. D. T.

A. M. Lale, J. D. T. Mason, and N. S. Jones, “Mucociliary transport and its assessment: a review,” Clin. Otolaryng. Allied Sci. 23(5), 388–396 (1998).
[Crossref]

Mazur, M.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Merhi, L. K.

Moninger, T. O.

A. S. Shah, Y. Ben-Shahar, T. O. Moninger, J. N. Kline, and M. J. Welsh, “Motile cilia of human airway epithelia are chemosensory,” Science 325(5944), 1131–1134 (2009).
[Crossref] [PubMed]

Myrtus, C.

Nevo, U.

I. Shock, A. Barbul, P. Girshovitz, U. Nevo, R. Korenstein, and N. T. Shakeda, “Optical phase nanoscopy in red blood cells using low-coherence spectroscopy,” J. Biomed. Opt. 17(10), 101509 (2012).
[Crossref] [PubMed]

Nezam, S. M. M.

Oldenburg, A. L.

Owen, G.

Özkumurc, E.

C. Joo, E. Özkumurc, M. S. Ünlüc, and J. F. de Boer, “Spectral-domain optical coherence phase microscopy for labelfree multiplexed protein microarray assay,” Biosens. and Bioelectron. 25(2), 275–281 (2009).
[Crossref]

Park, B. H.

Petersen, F.

S. Bermbach, K. Weinhold, T. Roeder, F. Petersen, C. Kugler, T. Goldmann, J. Rupp, and P. König, “Mechanisms of cilia-driven transport in the airways in the absence of mucus,” Am. J. Respir. Cell. Mol. Biol. 51(1), 56–67 (2014).
[Crossref] [PubMed]

Roeder, T.

S. Bermbach, K. Weinhold, T. Roeder, F. Petersen, C. Kugler, T. Goldmann, J. Rupp, and P. König, “Mechanisms of cilia-driven transport in the airways in the absence of mucus,” Am. J. Respir. Cell. Mol. Biol. 51(1), 56–67 (2014).
[Crossref] [PubMed]

Rowe, S. M.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Rupp, J.

S. Bermbach, K. Weinhold, T. Roeder, F. Petersen, C. Kugler, T. Goldmann, J. Rupp, and P. König, “Mechanisms of cilia-driven transport in the airways in the absence of mucus,” Am. J. Respir. Cell. Mol. Biol. 51(1), 56–67 (2014).
[Crossref] [PubMed]

Sanderson, M. J.

P. Delmotte and M. J. Sanderson, “Ciliary beat frequency is maintained at a maximal rate in the small airways of mouse lung slices,” Am. J. Respir. Cell. Mol. Biol. 35(1), 110–117 (2006).
[Crossref] [PubMed]

Sarunic, M. V.

Schuster, B. S.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

Schweikard, A.

Shah, A. S.

A. S. Shah, Y. Ben-Shahar, T. O. Moninger, J. N. Kline, and M. J. Welsh, “Motile cilia of human airway epithelia are chemosensory,” Science 325(5944), 1131–1134 (2009).
[Crossref] [PubMed]

Shakeda, N. T.

I. Shock, A. Barbul, P. Girshovitz, U. Nevo, R. Korenstein, and N. T. Shakeda, “Optical phase nanoscopy in red blood cells using low-coherence spectroscopy,” J. Biomed. Opt. 17(10), 101509 (2012).
[Crossref] [PubMed]

Sharma, N.

N. Sharma, N. F. Berbari, and B. K. Yoder, “Ciliary dysfunction in developmental abnormalities and diseases,” Curr. Top. Dev. Biol. 85, 371–427 (2008).

Shastry, S.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Shock, I.

I. Shock, A. Barbul, P. Girshovitz, U. Nevo, R. Korenstein, and N. T. Shakeda, “Optical phase nanoscopy in red blood cells using low-coherence spectroscopy,” J. Biomed. Opt. 17(10), 101509 (2012).
[Crossref] [PubMed]

Sleigh, M. A.

M. A. Sleigh, J. R. Blake, and N. Liron, “The propulsion of mucus by cilia,” Am. Rev. Respir. Dis. 137(3), 726–741 (1988).
[Crossref] [PubMed]

Smith, A. T.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

Sorscher, E. J.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

St. Quintin, A.

Swanson, E.

Tabrizian, M.

P. O. Bagnaninchi, C. Holmes, and M. Tabrizian, “Monitoring cells in engineered tissues with optical coherence phase microscopy: Optical phase fluctuations as endogenous sources of contrast,” Proc. SPIE 8580, 85800E (2013).

Tearney, G. J.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

S. M. M. Nezam, C. Joo, G. J. Tearney, and J. F. de Boer, “Application of maximum likelihood estimator in nano-scale optical path length measurement using spectral-domain optical coherence phasemicroscopy,” Opt. Express 16(22), 17186–17195 (2008).
[Crossref]

Ünlüc, M. S.

C. Joo, E. Özkumurc, M. S. Ünlüc, and J. F. de Boer, “Spectral-domain optical coherence phase microscopy for labelfree multiplexed protein microarray assay,” Biosens. and Bioelectron. 25(2), 275–281 (2009).
[Crossref]

Watson, J. D.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

Weinhold, K.

S. Bermbach, K. Weinhold, T. Roeder, F. Petersen, C. Kugler, T. Goldmann, J. Rupp, and P. König, “Mechanisms of cilia-driven transport in the airways in the absence of mucus,” Am. J. Respir. Cell. Mol. Biol. 51(1), 56–67 (2014).
[Crossref] [PubMed]

Welsh, M. J.

A. S. Shah, Y. Ben-Shahar, T. O. Moninger, J. N. Kline, and M. J. Welsh, “Motile cilia of human airway epithelia are chemosensory,” Science 325(5944), 1131–1134 (2009).
[Crossref] [PubMed]

Wess, J.

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

Wilsterman, E. J.

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Yang, C.

Yazdanfar, S.

M. A. Choma, A. K. Ellerbee, S. Yazdanfar, and J. A. Izatt, “Doppler flow imaging of cytoplasmic streaming using spectral domain phase microscopy,” J. Biomed. Opt. 11(2), 024014 (2006).
[Crossref] [PubMed]

Yoder, B. K.

N. Sharma, N. F. Berbari, and B. K. Yoder, “Ciliary dysfunction in developmental abnormalities and diseases,” Curr. Top. Dev. Biol. 85, 371–427 (2008).

Yos, H. J.

B. W. Bisgrove and H. J. Yos, “The roles of cilia in developmental disorders and disease,” Development 133(21), 4131–4143 (2006).
[Crossref] [PubMed]

Am. J. Respir. Cell. Mol. Biol. (2)

S. Bermbach, K. Weinhold, T. Roeder, F. Petersen, C. Kugler, T. Goldmann, J. Rupp, and P. König, “Mechanisms of cilia-driven transport in the airways in the absence of mucus,” Am. J. Respir. Cell. Mol. Biol. 51(1), 56–67 (2014).
[Crossref] [PubMed]

P. Delmotte and M. J. Sanderson, “Ciliary beat frequency is maintained at a maximal rate in the small airways of mouse lung slices,” Am. J. Respir. Cell. Mol. Biol. 35(1), 110–117 (2006).
[Crossref] [PubMed]

Am. J. Respir. Crit. Care. Med. (1)

S. E. Birket, K. K. Chu, L. Liu, G. H. Houser, B. J. Diephuis, E. J. Wilsterman, G. Dierksen, M. Mazur, S. Shastry, Y. Li, J. D. Watson, A. T. Smith, B. S. Schuster, J. Hanes, W. E. Grizzle, E. J. Sorscher, G. J. Tearney, and S. M. Rowe, “A functional anatomic defect of the cystic fibrosis airway,” Am. J. Respir. Crit. Care. Med. 190(4), 421–432 (2014).
[Crossref] [PubMed]

Am. Rev. Respir. Dis. (1)

M. A. Sleigh, J. R. Blake, and N. Liron, “The propulsion of mucus by cilia,” Am. Rev. Respir. Dis. 137(3), 726–741 (1988).
[Crossref] [PubMed]

Appl. Opt. (1)

Biomed. Opt. Express (2)

Biosens. and Bioelectron. (1)

C. Joo, E. Özkumurc, M. S. Ünlüc, and J. F. de Boer, “Spectral-domain optical coherence phase microscopy for labelfree multiplexed protein microarray assay,” Biosens. and Bioelectron. 25(2), 275–281 (2009).
[Crossref]

Clin. Otolaryng. Allied Sci. (1)

A. M. Lale, J. D. T. Mason, and N. S. Jones, “Mucociliary transport and its assessment: a review,” Clin. Otolaryng. Allied Sci. 23(5), 388–396 (1998).
[Crossref]

Curr. Top. Dev. Biol. (1)

N. Sharma, N. F. Berbari, and B. K. Yoder, “Ciliary dysfunction in developmental abnormalities and diseases,” Curr. Top. Dev. Biol. 85, 371–427 (2008).

Development (1)

B. W. Bisgrove and H. J. Yos, “The roles of cilia in developmental disorders and disease,” Development 133(21), 4131–4143 (2006).
[Crossref] [PubMed]

Eur. Respir. J. (1)

M. K. Klein, R. V. Haberberger, P. Hartmann, P. Faulhammer, K. S. Lips, B. Krain, J. Wess, W. Kummer, and P. König, “Muscarinic receptor subtypes in cilia-driven transport and airway epithelial development,” Eur. Respir. J. 33(5), 1113–1121 (2009).
[Crossref] [PubMed]

J. Biomed. Opt. (2)

I. Shock, A. Barbul, P. Girshovitz, U. Nevo, R. Korenstein, and N. T. Shakeda, “Optical phase nanoscopy in red blood cells using low-coherence spectroscopy,” J. Biomed. Opt. 17(10), 101509 (2012).
[Crossref] [PubMed]

M. A. Choma, A. K. Ellerbee, S. Yazdanfar, and J. A. Izatt, “Doppler flow imaging of cytoplasmic streaming using spectral domain phase microscopy,” J. Biomed. Opt. 11(2), 024014 (2006).
[Crossref] [PubMed]

Opt. Express (1)

Opt. Lett. (4)

PLoS One (1)

L. Liu, K. K. Chu, G. H. Houser, B. J. Diephuis, Y. Li, E. J. Wilsterman, S. Shastry, G. Dierksen, S. E. Birket, M. Mazur, S. Byan-Parker, W. E. Grizzle, E. J. Sorscher, S. M. Rowe, and G. J. Tearney, “Method for quantitative study of airway functional microanatomy using micro-optical coherence tomography,” PLoS One 8(1), e54473 (2013).
[PubMed]

Proc. SPIE (1)

P. O. Bagnaninchi, C. Holmes, and M. Tabrizian, “Monitoring cells in engineered tissues with optical coherence phase microscopy: Optical phase fluctuations as endogenous sources of contrast,” Proc. SPIE 8580, 85800E (2013).

Science (1)

A. S. Shah, Y. Ben-Shahar, T. O. Moninger, J. N. Kline, and M. J. Welsh, “Motile cilia of human airway epithelia are chemosensory,” Science 325(5944), 1131–1134 (2009).
[Crossref] [PubMed]

Supplementary Material (3)

NameDescription
» Visualization 1: AVI (3393 KB)     
» Visualization 2: AVI (650 KB)     
» Visualization 3: AVI (759 KB)     

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Figures (4)

Fig. 1
Fig. 1

(a) H&E stained histology of trachea cross-section, (b) Scanning electron microscope image of ciliated cells.

Fig. 2
Fig. 2

En face images (128 μm × 128 μm) of ex-vivo mouse trachea at different depth positions, with 0.25 μm/pixel display resolution. (a) Ciliated epithelium with individual cilia slightly blurred because of their coordinated beating. (b) and (c) Different cell layers beneath the ciliated cells. (d) and (e) Connective tissue layer. (f) Longitudinal cross-section of blood capillary where single red blood cells can be visualized (marked with red arrow). (g) and (h) Collagen fibres of the connective tissue. (i) Reconstructed three dimensional structure of tracheal epithelium, also shown in Visualization 1. Scale bar represents 20 μm.

Fig. 3
Fig. 3

High-speed volumetric imaging of mouse tracheal epithelium with SD-OCM. (a) Still image from Visualization 2 which shows volume of size 128 μm × 128 μm × 30 μm acquired at 1 volumes/sec. (b) Still image from Visualization 3 which shows volume of size 30 μm × 30 μm × 30 μm acquired at 108 volumes/sec.

Fig. 4
Fig. 4

(a) OPL values over time along a line in the y-direction in Fig. 3(b). (b) Gradient vectors representing the directional changes in OPL values. (c) OPL values over time at position marked by the dashed lines in (a). (d) Frequency spectrum of the OPL values over time.

Equations (1)

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O P L ( x , y ) = u . x ^ + v . y ^ u = δ δ x ( O P L ( x , y ) ) v = δ δ y ( O P L ( x , y ) )

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