Abstract

Pulmonary alveoli have been studied for many years, yet no unifying hypothesis exists for their dynamic mechanics during respiration due to their miniature size (100-300 μm dimater in humans) and constant motion, which prevent standard imaging techniques from visualizing four-dimensional dynamics of individual alveoli in vivo. Here we report a new platform to image the first layer of air-filled subpleural alveoli through the use of a lightweight optical frequency domain imaging (OFDI) probe that can be placed upon the pleura to move with the lung over the complete range of respiratory motion. This device enables in-vivo acquisition of four-dimensional microscopic images of alveolar airspaces (alveoli and ducts), within the same field of view, during continuous ventilation without restricting the motion or modifying the structure of the alveoli. Results from an exploratory study including three live swine suggest that subpleural alveolar air spaces are best fit with a uniform expansion (r2 = 0.98) over a recruitment model (r2 = 0.72). Simultaneously, however, the percentage change in volume shows heterogeneous alveolar expansion within just a 1 mm x 1 mm field of view. These results signify the importance of four-dimensional imaging tools, such as the device presented here. Quantification of the dynamic response of the lung during ventilation may help create more accurate modeling techniques and move toward a more complete understanding of alveolar mechanics.

© 2013 Optical Society of America

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    [CrossRef] [PubMed]
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  35. R. R. Mercer, J. M. Laco, J. D. Crapo, “Three-dimensional reconstruction of alveoli in the rat lung for pressure-volume relationships,” J. Appl. Physiol. 62(4), 1480–1487 (1987).
    [PubMed]
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    [CrossRef] [PubMed]
  37. J. Gil, E. R. Weibel, “Morphological study of pressure-volume hysteresis in rat lungs fixed by vascular perfusion,” Respir. Physiol. 15(2), 190–213 (1972).
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    [PubMed]
  43. H. Bachofen, S. Schürch, M. Urbinelli, E. R. Weibel, “Relations among alveolar surface tension, surface area, volume, and recoil pressure,” J. Appl. Physiol. 62(5), 1878–1887 (1987).
    [PubMed]
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2013

L. Kirsten, M. Gaertner, C. Schnabel, S. Meissner, E. Koch, “Four-dimensional imaging of murine subpleural alveoli using high-speed optical coherence tomography,” J. Biophotonics 6(2), 148–152 (2013).
[CrossRef] [PubMed]

2012

C. I. Unglert, E. Namati, W. C. Warger, L. Liu, H. Yoo, D. K. Kang, B. E. Bouma, G. J. Tearney, “Evaluation of optical reflectance techniques for imaging of alveolar structure,” J. Biomed. Opt. 17(7), 071303 (2012).
[CrossRef] [PubMed]

Y. Wu, C. E. Perlman, “In situ methods for assessing alveolar mechanics,” J. Appl. Physiol. 112(3), 519–526 (2012).
[CrossRef] [PubMed]

C. I. Unglert, W. C. Warger, J. Hostens, E. Namati, R. Birngruber, B. E. Bouma, G. J. Tearney, “Validation of two-dimensional and three-dimensional measurements of subpleural alveolar size parameters by optical coherence tomography,” J. Biomed. Opt. 17(12), 126015 (2012).
[CrossRef] [PubMed]

A. J. Hajari, D. A. Yablonskiy, A. L. Sukstanskii, J. D. Quirk, M. S. Conradi, J. C. Woods, “Morphometric changes in the human pulmonary acinus during inflation,” J. Appl. Physiol. 112(6), 937–943 (2012).
[CrossRef] [PubMed]

R. A. McLaughlin, X. Yang, B. C. Quirk, D. Lorenser, R. W. Kirk, P. B. Noble, D. D. Sampson, “Static and dynamic imaging of alveoli using optical coherence tomography needle probes,” J. Appl. Physiol. 113(6), 967–974 (2012).
[CrossRef] [PubMed]

2011

M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8(1), 91–96 (2011).
[CrossRef] [PubMed]

E. Roan, C. M. Waters, “What do we know about mechanical strain in lung alveoli?” Am. J. Physiol. Lung Cell. Mol. Physiol. 301(5), L625–L635 (2011).
[CrossRef] [PubMed]

M. Cereda, K. Emami, S. Kadlecek, Y. Xin, P. Mongkolwisetwara, H. Profka, A. Barulic, S. Pickup, S. Månsson, P. Wollmer, M. Ishii, C. S. Deutschman, R. R. Rizi, “Quantitative imaging of alveolar recruitment with hyperpolarized gas MRI during mechanical ventilation,” J. Appl. Physiol. 110(2), 499–511 (2011).
[CrossRef] [PubMed]

D. Schwenninger, H. Runck, S. Schumann, J. Haberstroh, S. Meissner, E. Koch, J. Guttmann, “Intravital microscopy of subpleural alveoli via transthoracic endoscopy,” J. Biomed. Opt. 16(4), 046002 (2011).
[CrossRef] [PubMed]

H. Liu, H. Runck, M. Schneider, X. Tong, C. A. Stahl, “Morphometry of subpleural alveoli may be greatly biased by local pressure changes induced by the microscopic device,” Respir. Physiol. Neurobiol. 178(2), 283–289 (2011).
[CrossRef] [PubMed]

2010

S. Meissner, L. Knels, C. Schnabel, T. Koch, E. Koch, “Three-dimensional Fourier domain optical coherence tomography in vivo imaging of alveolar tissue in the intact thorax using the parietal pleura as a window,” J. Biomed. Opt. 15(1), 016030 (2010).
[CrossRef] [PubMed]

S. Meissner, A. Tabuchi, M. Mertens, W. M. Kuebler, E. Koch, “Virtual four-dimensional imaging of lung parenchyma by optical coherence tomography in mice,” J. Biomed. Opt. 15(3), 036016 (2010).
[CrossRef] [PubMed]

2009

M. Mertens, A. Tabuchi, S. Meissner, A. Krueger, K. Schirrmann, U. Kertzscher, A. R. Pries, A. S. Slutsky, E. Koch, W. M. Kuebler, “Alveolar dynamics in acute lung injury: heterogeneous distension rather than cyclic opening and collapse,” Crit. Care Med. 37(9), 2604–2611 (2009).
[CrossRef] [PubMed]

D. A. Yablonskiy, A. L. Sukstanskii, J. C. Woods, D. S. Gierada, J. D. Quirk, J. C. Hogg, J. D. Cooper, M. S. Conradi, “Quantification of lung microstructure with hyperpolarized 3He diffusion MRI,” J. Appl. Physiol. 107(4), 1258–1265 (2009).
[CrossRef] [PubMed]

J. Bickenbach, R. Dembinski, M. Czaplik, S. Meissner, A. Tabuchi, M. Mertens, L. Knels, W. Schroeder, P. Pelosi, E. Koch, W. M. Kuebler, R. Rossaint, R. Kuhlen, “Comparison of two in vivo microscopy techniques to visualize alveolar mechanics,” J. Clin. Monit. Comput. 23(5), 323–332 (2009).
[CrossRef] [PubMed]

S. Meissner, L. Knels, E. Koch, “Improved three-dimensional Fourier domain optical coherence tomography by index matching in alveolar structures,” J. Biomed. Opt. 14(6), 064037 (2009).
[CrossRef] [PubMed]

2007

S. H. Yun, G. J. Tearney, B. J. Vakoc, M. Shishkov, W. Y. Oh, A. E. Desjardins, M. J. Suter, R. C. Chan, J. A. Evans, I.-K. Jang, N. S. Nishioka, J. F. de Boer, B. E. Bouma, “Comprehensive volumetric optical microscopy in vivo,” Nat. Med. 12(12), 1429–1433 (2007).
[CrossRef] [PubMed]

E. Namati, J. De Ryk, J. Thiesse, Z. Towfic, E. Hoffman, G. Mclennan, “Large image microscope array for the compilation of multimodality whole organ image databases,” Anat. Rec. (Hoboken) 290(11), 1377–1387 (2007).
[CrossRef] [PubMed]

2006

C. A. Stahl, K. Möller, S. Schumann, R. Kuhlen, M. Sydow, C. Putensen, J. Guttmann, “Dynamic versus static respiratory mechanics in acute lung injury and acute respiratory distress syndrome,” Crit. Care Med. 34(8), 2090–2098 (2006).
[CrossRef] [PubMed]

J. D. DiRocco, L. A. Pavone, D. E. Carney, C. J. Lutz, L. A. Gatto, S. K. Landas, G. F. Nieman, “Dynamic alveolar mechanics in four models of lung injury,” Intensive Care Med. 32(1), 140–148 (2006).
[CrossRef] [PubMed]

2005

R. S. Harris, “Pressure-volume curves of the respiratory system,” Respir. Care 50(1), 78–98, discussion 98–99 (2005).
[PubMed]

N. Hanna, D. Saltzman, D. Mukai, Z. Chen, S. Sasse, J. Milliken, S. Guo, W. Jung, H. Colt, M. Brenner, “Two-dimensional and 3-dimensional optical coherence tomographic imaging of the airway, lung, and pleura,” J. Thorac. Cardiovasc. Surg. 129(3), 615–622 (2005).
[CrossRef] [PubMed]

2004

J. M. Steinberg, H. J. Schiller, J. M. Halter, L. A. Gatto, H.-M. Lee, L. A. Pavone, G. F. Nieman, “Alveolar instability causes early ventilator-induced lung injury independent of neutrophils,” Am. J. Respir. Crit. Care Med. 169(1), 57–63 (2004).
[CrossRef] [PubMed]

2003

2002

J. Steinberg, H. J. Schiller, J. M. Halter, L. A. Gatto, M. Dasilva, M. Amato, U. G. McCann, G. F. Nieman, “Tidal volume increases do not affect alveolar mechanics in normal lung but cause alveolar overdistension and exacerbate alveolar instability after surfactant deactivation,” Crit. Care Med. 30(12), 2675–2683 (2002).
[CrossRef] [PubMed]

2001

H. J. Schiller, U. G. McCann, D. E. Carney, L. A. Gatto, J. M. Steinberg, G. F. Nieman, “Altered alveolar mechanics in the acutely injured lung,” Crit. Care Med. 29(5), 1049–1055 (2001).
[CrossRef] [PubMed]

1999

D. E. Carney, C. E. Bredenberg, H. J. Schiller, A. L. Picone, U. E. McCann, L. A. Gatto, G. Bailey, M. Fillinger, G. F. Nieman, “The mechanism of lung volume change during mechanical ventilation,” Am. J. Respir. Crit. Care Med. 160(5), 1697–1702 (1999).
[CrossRef]

1998

J. G. Venegas, R. S. Harris, B. A. Simon, “A comprehensive equation for the pulmonary pressure-volume curve,” J. Appl. Physiol. 84(1), 389–395 (1998).
[PubMed]

1995

J. Bastacky, C. Y. C. Lee, J. Goerke, H. Koushafar, D. Yager, L. Kenaga, T. P. Speed, Y. Chen, J. A. Clements, “Alveolar lining layer is thin and continuous: low-temperature scanning electron microscopy of rat lung,” J. Appl. Physiol. 79(5), 1615–1628 (1995).
[PubMed]

1992

R. P. Woods, S. R. Cherry, J. C. Mazziotta, “Rapid automated algorithm for aligning and reslicing PET images,” J. Comput. Assist. Tomogr. 16(4), 620–633 (1992).
[CrossRef] [PubMed]

1991

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

E. H. Oldmixon, F. G. Hoppin., “Alveolar septal folding and lung inflation history,” J. Appl. Physiol. 71(6), 2369–2379 (1991).
[PubMed]

1987

H. Bachofen, S. Schürch, M. Urbinelli, E. R. Weibel, “Relations among alveolar surface tension, surface area, volume, and recoil pressure,” J. Appl. Physiol. 62(5), 1878–1887 (1987).
[PubMed]

R. R. Mercer, J. M. Laco, J. D. Crapo, “Three-dimensional reconstruction of alveoli in the rat lung for pressure-volume relationships,” J. Appl. Physiol. 62(4), 1480–1487 (1987).
[PubMed]

1981

G. F. Nieman, C. E. Bredenberg, W. R. Clark, N. R. West, “Alveolar function following surfactant deactivation,” J. Appl. Physiol. 51(4), 895–904 (1981).
[PubMed]

1979

J. Gil, H. Bachofen, P. Gehr, E. R. Weibel, “Alveolar volume-surface area relation in air- and saline-filled lungs fixed by vascular perfusion,” J. Appl. Physiol. 47(5), 990–1001 (1979).
[PubMed]

1976

A. Assimacopoulos, R. Guggenheim, Y. Kapanci, “Changes in alveolar capillary configuration at different levels of lung inflation in the rat. An ultrastructural and morphometric study,” Lab. Invest. 34(1), 10–22 (1976).
[PubMed]

1975

B. D. T. Daly, G. E. Parks, C. H. Edmonds, C. W. Hibbs, J. C. Norman, “Dynamic alveolar mechanics as studied by videomicroscopy,” Respir. Physiol. 24(2), 217–232 (1975).
[CrossRef] [PubMed]

1973

A. P. Moreci, J. C. Norman, “Measurements of alveolar sac diameters by incident-light photomicrography. effects of positive-pressure respiration,” Ann. Thorac. Surg. 15(2), 179–186 (1973).
[CrossRef] [PubMed]

1972

E. D’Angelo, “Local alveolar size and transpulmonary pressure in situ and in isolated lungs,” Respir. Physiol. 14(3), 251–266 (1972).
[CrossRef] [PubMed]

J. Gil, E. R. Weibel, “Morphological study of pressure-volume hysteresis in rat lungs fixed by vascular perfusion,” Respir. Physiol. 15(2), 190–213 (1972).
[CrossRef] [PubMed]

1969

W. W. Wagner., “Pulmonary microcirculatory observations in vivo under physiological conditions,” J. Appl. Physiol. 26(3), 375–377 (1969).
[PubMed]

1946

H. Rahn, A. B. Otis, L. E. Chadwick, W. O. Fenn, “The pressure-volume diagram of the thorax and lung,” Am. J. Physiol. 146(2), 161–178 (1946).
[PubMed]

Amato, M.

J. Steinberg, H. J. Schiller, J. M. Halter, L. A. Gatto, M. Dasilva, M. Amato, U. G. McCann, G. F. Nieman, “Tidal volume increases do not affect alveolar mechanics in normal lung but cause alveolar overdistension and exacerbate alveolar instability after surfactant deactivation,” Crit. Care Med. 30(12), 2675–2683 (2002).
[CrossRef] [PubMed]

Assimacopoulos, A.

A. Assimacopoulos, R. Guggenheim, Y. Kapanci, “Changes in alveolar capillary configuration at different levels of lung inflation in the rat. An ultrastructural and morphometric study,” Lab. Invest. 34(1), 10–22 (1976).
[PubMed]

Bachofen, H.

H. Bachofen, S. Schürch, M. Urbinelli, E. R. Weibel, “Relations among alveolar surface tension, surface area, volume, and recoil pressure,” J. Appl. Physiol. 62(5), 1878–1887 (1987).
[PubMed]

J. Gil, H. Bachofen, P. Gehr, E. R. Weibel, “Alveolar volume-surface area relation in air- and saline-filled lungs fixed by vascular perfusion,” J. Appl. Physiol. 47(5), 990–1001 (1979).
[PubMed]

Bailey, G.

D. E. Carney, C. E. Bredenberg, H. J. Schiller, A. L. Picone, U. E. McCann, L. A. Gatto, G. Bailey, M. Fillinger, G. F. Nieman, “The mechanism of lung volume change during mechanical ventilation,” Am. J. Respir. Crit. Care Med. 160(5), 1697–1702 (1999).
[CrossRef]

Barulic, A.

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M. Cereda, K. Emami, S. Kadlecek, Y. Xin, P. Mongkolwisetwara, H. Profka, A. Barulic, S. Pickup, S. Månsson, P. Wollmer, M. Ishii, C. S. Deutschman, R. R. Rizi, “Quantitative imaging of alveolar recruitment with hyperpolarized gas MRI during mechanical ventilation,” J. Appl. Physiol. 110(2), 499–511 (2011).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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C. A. Stahl, K. Möller, S. Schumann, R. Kuhlen, M. Sydow, C. Putensen, J. Guttmann, “Dynamic versus static respiratory mechanics in acute lung injury and acute respiratory distress syndrome,” Crit. Care Med. 34(8), 2090–2098 (2006).
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R. A. McLaughlin, X. Yang, B. C. Quirk, D. Lorenser, R. W. Kirk, P. B. Noble, D. D. Sampson, “Static and dynamic imaging of alveoli using optical coherence tomography needle probes,” J. Appl. Physiol. 113(6), 967–974 (2012).
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A. J. Hajari, D. A. Yablonskiy, A. L. Sukstanskii, J. D. Quirk, M. S. Conradi, J. C. Woods, “Morphometric changes in the human pulmonary acinus during inflation,” J. Appl. Physiol. 112(6), 937–943 (2012).
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E. Roan, C. M. Waters, “What do we know about mechanical strain in lung alveoli?” Am. J. Physiol. Lung Cell. Mol. Physiol. 301(5), L625–L635 (2011).
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J. Bickenbach, R. Dembinski, M. Czaplik, S. Meissner, A. Tabuchi, M. Mertens, L. Knels, W. Schroeder, P. Pelosi, E. Koch, W. M. Kuebler, R. Rossaint, R. Kuhlen, “Comparison of two in vivo microscopy techniques to visualize alveolar mechanics,” J. Clin. Monit. Comput. 23(5), 323–332 (2009).
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H. Liu, H. Runck, M. Schneider, X. Tong, C. A. Stahl, “Morphometry of subpleural alveoli may be greatly biased by local pressure changes induced by the microscopic device,” Respir. Physiol. Neurobiol. 178(2), 283–289 (2011).
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R. A. McLaughlin, X. Yang, B. C. Quirk, D. Lorenser, R. W. Kirk, P. B. Noble, D. D. Sampson, “Static and dynamic imaging of alveoli using optical coherence tomography needle probes,” J. Appl. Physiol. 113(6), 967–974 (2012).
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J. M. Steinberg, H. J. Schiller, J. M. Halter, L. A. Gatto, H.-M. Lee, L. A. Pavone, G. F. Nieman, “Alveolar instability causes early ventilator-induced lung injury independent of neutrophils,” Am. J. Respir. Crit. Care Med. 169(1), 57–63 (2004).
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H. J. Schiller, U. G. McCann, D. E. Carney, L. A. Gatto, J. M. Steinberg, G. F. Nieman, “Altered alveolar mechanics in the acutely injured lung,” Crit. Care Med. 29(5), 1049–1055 (2001).
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M. Mertens, A. Tabuchi, S. Meissner, A. Krueger, K. Schirrmann, U. Kertzscher, A. R. Pries, A. S. Slutsky, E. Koch, W. M. Kuebler, “Alveolar dynamics in acute lung injury: heterogeneous distension rather than cyclic opening and collapse,” Crit. Care Med. 37(9), 2604–2611 (2009).
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L. Kirsten, M. Gaertner, C. Schnabel, S. Meissner, E. Koch, “Four-dimensional imaging of murine subpleural alveoli using high-speed optical coherence tomography,” J. Biophotonics 6(2), 148–152 (2013).
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H. Liu, H. Runck, M. Schneider, X. Tong, C. A. Stahl, “Morphometry of subpleural alveoli may be greatly biased by local pressure changes induced by the microscopic device,” Respir. Physiol. Neurobiol. 178(2), 283–289 (2011).
[CrossRef] [PubMed]

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J. Bickenbach, R. Dembinski, M. Czaplik, S. Meissner, A. Tabuchi, M. Mertens, L. Knels, W. Schroeder, P. Pelosi, E. Koch, W. M. Kuebler, R. Rossaint, R. Kuhlen, “Comparison of two in vivo microscopy techniques to visualize alveolar mechanics,” J. Clin. Monit. Comput. 23(5), 323–332 (2009).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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D. Schwenninger, H. Runck, S. Schumann, J. Haberstroh, S. Meissner, E. Koch, J. Guttmann, “Intravital microscopy of subpleural alveoli via transthoracic endoscopy,” J. Biomed. Opt. 16(4), 046002 (2011).
[CrossRef] [PubMed]

C. A. Stahl, K. Möller, S. Schumann, R. Kuhlen, M. Sydow, C. Putensen, J. Guttmann, “Dynamic versus static respiratory mechanics in acute lung injury and acute respiratory distress syndrome,” Crit. Care Med. 34(8), 2090–2098 (2006).
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H. Bachofen, S. Schürch, M. Urbinelli, E. R. Weibel, “Relations among alveolar surface tension, surface area, volume, and recoil pressure,” J. Appl. Physiol. 62(5), 1878–1887 (1987).
[PubMed]

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D. Schwenninger, H. Runck, S. Schumann, J. Haberstroh, S. Meissner, E. Koch, J. Guttmann, “Intravital microscopy of subpleural alveoli via transthoracic endoscopy,” J. Biomed. Opt. 16(4), 046002 (2011).
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M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8(1), 91–96 (2011).
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H. Liu, H. Runck, M. Schneider, X. Tong, C. A. Stahl, “Morphometry of subpleural alveoli may be greatly biased by local pressure changes induced by the microscopic device,” Respir. Physiol. Neurobiol. 178(2), 283–289 (2011).
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C. A. Stahl, K. Möller, S. Schumann, R. Kuhlen, M. Sydow, C. Putensen, J. Guttmann, “Dynamic versus static respiratory mechanics in acute lung injury and acute respiratory distress syndrome,” Crit. Care Med. 34(8), 2090–2098 (2006).
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J. Steinberg, H. J. Schiller, J. M. Halter, L. A. Gatto, M. Dasilva, M. Amato, U. G. McCann, G. F. Nieman, “Tidal volume increases do not affect alveolar mechanics in normal lung but cause alveolar overdistension and exacerbate alveolar instability after surfactant deactivation,” Crit. Care Med. 30(12), 2675–2683 (2002).
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J. M. Steinberg, H. J. Schiller, J. M. Halter, L. A. Gatto, H.-M. Lee, L. A. Pavone, G. F. Nieman, “Alveolar instability causes early ventilator-induced lung injury independent of neutrophils,” Am. J. Respir. Crit. Care Med. 169(1), 57–63 (2004).
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H. J. Schiller, U. G. McCann, D. E. Carney, L. A. Gatto, J. M. Steinberg, G. F. Nieman, “Altered alveolar mechanics in the acutely injured lung,” Crit. Care Med. 29(5), 1049–1055 (2001).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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A. J. Hajari, D. A. Yablonskiy, A. L. Sukstanskii, J. D. Quirk, M. S. Conradi, J. C. Woods, “Morphometric changes in the human pulmonary acinus during inflation,” J. Appl. Physiol. 112(6), 937–943 (2012).
[CrossRef] [PubMed]

D. A. Yablonskiy, A. L. Sukstanskii, J. C. Woods, D. S. Gierada, J. D. Quirk, J. C. Hogg, J. D. Cooper, M. S. Conradi, “Quantification of lung microstructure with hyperpolarized 3He diffusion MRI,” J. Appl. Physiol. 107(4), 1258–1265 (2009).
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S. H. Yun, G. J. Tearney, B. J. Vakoc, M. Shishkov, W. Y. Oh, A. E. Desjardins, M. J. Suter, R. C. Chan, J. A. Evans, I.-K. Jang, N. S. Nishioka, J. F. de Boer, B. E. Bouma, “Comprehensive volumetric optical microscopy in vivo,” Nat. Med. 12(12), 1429–1433 (2007).
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C. A. Stahl, K. Möller, S. Schumann, R. Kuhlen, M. Sydow, C. Putensen, J. Guttmann, “Dynamic versus static respiratory mechanics in acute lung injury and acute respiratory distress syndrome,” Crit. Care Med. 34(8), 2090–2098 (2006).
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S. Meissner, A. Tabuchi, M. Mertens, W. M. Kuebler, E. Koch, “Virtual four-dimensional imaging of lung parenchyma by optical coherence tomography in mice,” J. Biomed. Opt. 15(3), 036016 (2010).
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M. Mertens, A. Tabuchi, S. Meissner, A. Krueger, K. Schirrmann, U. Kertzscher, A. R. Pries, A. S. Slutsky, E. Koch, W. M. Kuebler, “Alveolar dynamics in acute lung injury: heterogeneous distension rather than cyclic opening and collapse,” Crit. Care Med. 37(9), 2604–2611 (2009).
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C. I. Unglert, W. C. Warger, J. Hostens, E. Namati, R. Birngruber, B. E. Bouma, G. J. Tearney, “Validation of two-dimensional and three-dimensional measurements of subpleural alveolar size parameters by optical coherence tomography,” J. Biomed. Opt. 17(12), 126015 (2012).
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C. I. Unglert, E. Namati, W. C. Warger, L. Liu, H. Yoo, D. K. Kang, B. E. Bouma, G. J. Tearney, “Evaluation of optical reflectance techniques for imaging of alveolar structure,” J. Biomed. Opt. 17(7), 071303 (2012).
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S. H. Yun, G. J. Tearney, B. J. Vakoc, M. Shishkov, W. Y. Oh, A. E. Desjardins, M. J. Suter, R. C. Chan, J. A. Evans, I.-K. Jang, N. S. Nishioka, J. F. de Boer, B. E. Bouma, “Comprehensive volumetric optical microscopy in vivo,” Nat. Med. 12(12), 1429–1433 (2007).
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M. R. Looney, E. E. Thornton, D. Sen, W. J. Lamm, R. W. Glenny, M. F. Krummel, “Stabilized imaging of immune surveillance in the mouse lung,” Nat. Methods 8(1), 91–96 (2011).
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H. Liu, H. Runck, M. Schneider, X. Tong, C. A. Stahl, “Morphometry of subpleural alveoli may be greatly biased by local pressure changes induced by the microscopic device,” Respir. Physiol. Neurobiol. 178(2), 283–289 (2011).
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E. Namati, J. De Ryk, J. Thiesse, Z. Towfic, E. Hoffman, G. Mclennan, “Large image microscope array for the compilation of multimodality whole organ image databases,” Anat. Rec. (Hoboken) 290(11), 1377–1387 (2007).
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C. I. Unglert, W. C. Warger, J. Hostens, E. Namati, R. Birngruber, B. E. Bouma, G. J. Tearney, “Validation of two-dimensional and three-dimensional measurements of subpleural alveolar size parameters by optical coherence tomography,” J. Biomed. Opt. 17(12), 126015 (2012).
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C. I. Unglert, E. Namati, W. C. Warger, L. Liu, H. Yoo, D. K. Kang, B. E. Bouma, G. J. Tearney, “Evaluation of optical reflectance techniques for imaging of alveolar structure,” J. Biomed. Opt. 17(7), 071303 (2012).
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H. Bachofen, S. Schürch, M. Urbinelli, E. R. Weibel, “Relations among alveolar surface tension, surface area, volume, and recoil pressure,” J. Appl. Physiol. 62(5), 1878–1887 (1987).
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S. H. Yun, G. J. Tearney, B. J. Vakoc, M. Shishkov, W. Y. Oh, A. E. Desjardins, M. J. Suter, R. C. Chan, J. A. Evans, I.-K. Jang, N. S. Nishioka, J. F. de Boer, B. E. Bouma, “Comprehensive volumetric optical microscopy in vivo,” Nat. Med. 12(12), 1429–1433 (2007).
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J. G. Venegas, R. S. Harris, B. A. Simon, “A comprehensive equation for the pulmonary pressure-volume curve,” J. Appl. Physiol. 84(1), 389–395 (1998).
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C. I. Unglert, W. C. Warger, J. Hostens, E. Namati, R. Birngruber, B. E. Bouma, G. J. Tearney, “Validation of two-dimensional and three-dimensional measurements of subpleural alveolar size parameters by optical coherence tomography,” J. Biomed. Opt. 17(12), 126015 (2012).
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C. I. Unglert, E. Namati, W. C. Warger, L. Liu, H. Yoo, D. K. Kang, B. E. Bouma, G. J. Tearney, “Evaluation of optical reflectance techniques for imaging of alveolar structure,” J. Biomed. Opt. 17(7), 071303 (2012).
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E. Roan, C. M. Waters, “What do we know about mechanical strain in lung alveoli?” Am. J. Physiol. Lung Cell. Mol. Physiol. 301(5), L625–L635 (2011).
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H. Bachofen, S. Schürch, M. Urbinelli, E. R. Weibel, “Relations among alveolar surface tension, surface area, volume, and recoil pressure,” J. Appl. Physiol. 62(5), 1878–1887 (1987).
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M. Cereda, K. Emami, S. Kadlecek, Y. Xin, P. Mongkolwisetwara, H. Profka, A. Barulic, S. Pickup, S. Månsson, P. Wollmer, M. Ishii, C. S. Deutschman, R. R. Rizi, “Quantitative imaging of alveolar recruitment with hyperpolarized gas MRI during mechanical ventilation,” J. Appl. Physiol. 110(2), 499–511 (2011).
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A. J. Hajari, D. A. Yablonskiy, A. L. Sukstanskii, J. D. Quirk, M. S. Conradi, J. C. Woods, “Morphometric changes in the human pulmonary acinus during inflation,” J. Appl. Physiol. 112(6), 937–943 (2012).
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M. Cereda, K. Emami, S. Kadlecek, Y. Xin, P. Mongkolwisetwara, H. Profka, A. Barulic, S. Pickup, S. Månsson, P. Wollmer, M. Ishii, C. S. Deutschman, R. R. Rizi, “Quantitative imaging of alveolar recruitment with hyperpolarized gas MRI during mechanical ventilation,” J. Appl. Physiol. 110(2), 499–511 (2011).
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A. J. Hajari, D. A. Yablonskiy, A. L. Sukstanskii, J. D. Quirk, M. S. Conradi, J. C. Woods, “Morphometric changes in the human pulmonary acinus during inflation,” J. Appl. Physiol. 112(6), 937–943 (2012).
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D. A. Yablonskiy, A. L. Sukstanskii, J. C. Woods, D. S. Gierada, J. D. Quirk, J. C. Hogg, J. D. Cooper, M. S. Conradi, “Quantification of lung microstructure with hyperpolarized 3He diffusion MRI,” J. Appl. Physiol. 107(4), 1258–1265 (2009).
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J. Bastacky, C. Y. C. Lee, J. Goerke, H. Koushafar, D. Yager, L. Kenaga, T. P. Speed, Y. Chen, J. A. Clements, “Alveolar lining layer is thin and continuous: low-temperature scanning electron microscopy of rat lung,” J. Appl. Physiol. 79(5), 1615–1628 (1995).
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R. A. McLaughlin, X. Yang, B. C. Quirk, D. Lorenser, R. W. Kirk, P. B. Noble, D. D. Sampson, “Static and dynamic imaging of alveoli using optical coherence tomography needle probes,” J. Appl. Physiol. 113(6), 967–974 (2012).
[CrossRef] [PubMed]

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C. I. Unglert, E. Namati, W. C. Warger, L. Liu, H. Yoo, D. K. Kang, B. E. Bouma, G. J. Tearney, “Evaluation of optical reflectance techniques for imaging of alveolar structure,” J. Biomed. Opt. 17(7), 071303 (2012).
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Figures (8)

Fig. 1
Fig. 1

Picture of the MEMS probe with a diagram of the primary components within the MEMS probe and the positioning on the right middle lobe of live swine on mechanical ventilation. An optical fiber and electrical cable connect the probe to the OFDI system.

Fig. 2
Fig. 2

(A) OFDI and (B) micro-CT axial cross sections of fixed subpleural swine alveoli. High correlation of segmented (C) volume (Vmicro-CT = 1.38VOFDI + 0.003) and (D) surface area (SAmicro-CT = 1.15SAOFDI + 0.0006) show relative measurements of subpleural alveolar dynamics can be measured accurately with OFDI. Scale bar = 200 μm.

Fig. 3
Fig. 3

(A) Non-contact bench-top and (B) contact MEMS-probe axial cross-sections of freshly excised subpleural swine alveoli. (C) High correlation of segmented volumes between contact and non-contact scanning systems (Vcontact = 1.48Vnon-contact + 3491) show the probe does not create remarkable difference in volume measurements. Scale bar = 100 μm.

Fig. 4
Fig. 4

(A) En-face and (B) axial cross-sectional OFDI images acquired over one respiratory cycle in vivo with swine continuously ventilated at 10 bpm, 3 cmH2O PEEP, 20 cmH2O PIP. (C) Four-dimensional rendering of 34 segmented subpleural alveolar air spaces. (D) Maximum intensity projection (MIP) en-face visualization of segmented alveoli color-coded to percentage volume change of each alveolar air space over the respiratory cycle. (E) Intratracheal pressure trace during the respiratory cycle where * denotes mean intratracheal pressure during the volume acquisition within 1.05 s. Scale bar = 100 μm.

Fig. 5
Fig. 5

Representative four-dimensional visualization of 34 subpleural alveolar air spaces over three breaths in healthy swine ventilated at 10 bpm, 3 cmH2O PEEP, and 20 cmH2O PIP. OFDI images were acquired with a lightweight probe placed directly upon pleura during a thoracotomy procedure (Media 1). The top-left panel is an en-face view and the bottom-left panel is an axial cross-sectional view from the OFDI data sets. The top-center panel provides an en-face view and the bottom-center panel provides an isometric view of the segmented alveolar air spaces. The top-right panel is a maximum intensity projection of the segmented alveoli within the en-face plane where the color represents the percent change in volume of each alveolar air space with respect to the minimum volume during the three breaths. It is important to note the heterogeneity of the alveolar expansion where some alveoli change volume with the change in pressure and others undergo minimal change. The bottom-right panel provides the pressure profile over the 3 respiratory cycles, where the asterisk (*) represents the mean pressure during the volume acquisition.

Fig. 6
Fig. 6

(A) Histogram of maximum ∆V% and (B) scatter plot of air space volume vs. intratracheal pressure during the acquisition show heterogeneous alveolar expansion within the 1 mm x 1 mm field of view of subpleural alveoli.

Fig. 7
Fig. 7

(A) Total ∆V% with respect to minimum volume during 3 respiratory cycles plotted against mean intratracheal pressure during volume acquisition shows immediate alveolar volume increase upon inhalation and delay in volume decrease upon exhalation. (B) Total lung PV curve from intratracheal pressure and flow shows representative hysteresis of complete lung during imaging. (C) Alveolar PV curve for all 34 subpleural alveolar air spaces during 3 respiratory cycles closely approximates the lung compliance curve. The PV-curve scatter plots were fit by the equation: V = a + b/[1-exp(-(P-c)/d)] where V is the Volume, P is the pressure, and a, b, c, d are fit parameters [33].

Fig. 8
Fig. 8

Logarithmic plot of SAT versus VT of subpleural swine alveoli within a 930 μm x 930 μm field of view continuously ventilated in vivo. (A) The best fit line was defined: log SAT = (0.660 ± 0.012) log VT + 0.027. (B) The comparison of pure recruitment (dashed blue line) and uniform expansion (solid red line) models reinforce that the subpleural alveolar dynamics were best fit with a uniform expansion model.

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