Abstract

We demonstrate a handheld multiphoton endomicroscope with 3.4 mm distal diameter that can repetitively image mouse colon in vivo. A 2D resonant MEMS mirror was developed to perform beam scanning in a Lissajous pattern. The instrument has an effective numerical aperture of 0.63, lateral and axial resolution of 2.03 and 9.02 μm, respectively, working distance of 60 μm, and image field-of-view of 300 × 300 μm2. Hoechst was injected intravenously in mice to stain cell nuclei. We were able to collect histology-like images in vivo at 5 frames/sec, and distinguish between normal and pre-malignant colonic epithelium.

© 2015 Optical Society of America

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2014 (3)

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

W. Shahid, Z. Qiu, X. Duan, H. Li, T. D. Wang, and K. R. Oldham, “Modeling and Simulation of a Parametrically Resonant Micromirror With Duty-Cycled Excitation,” J. Microelectromech. Syst. 23(6), 1440–1453 (2014).
[Crossref] [PubMed]

L. Ritsma, S. I. J. Ellenbroek, A. Zomer, H. J. Snippert, F. J. de Sauvage, B. D. Simons, H. Clevers, and J. van Rheenen, “Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging,” Nature 507(7492), 362–365 (2014).
[Crossref] [PubMed]

2013 (1)

2012 (4)

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. USA 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

D. M. Huland, C. M. Brown, S. S. Howard, D. G. Ouzounov, I. Pavlova, K. Wang, D. R. Rivera, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using long gradient index lens multiphoton endoscopic systems,” Biomed. Opt. Express 3(5), 1077–1085 (2012).
[Crossref] [PubMed]

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

A. Masedunskas, M. Sramkova, L. Parente, and R. Weigert, “Intravital Microscopy to Image Membrane Trafficking in Live Rats,” Methods Mol. Biol. 931, 153–167 (2012).
[Crossref] [PubMed]

2011 (2)

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17598–17603 (2011).
[Crossref] [PubMed]

C. L. Hoy, O. Ferhanoğlu, M. Yildirim, W. Piyawattanametha, H. Ra, O. Solgaard, and A. Ben-Yakar, “Optical design and imaging performance testing of a 9.6-mm diameter femtosecond laser microsurgery probe,” Opt. Express 19(11), 10536–10552 (2011).
[Crossref] [PubMed]

2009 (3)

2008 (1)

2007 (2)

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

T. Hinoi, A. Akyol, B. K. Theisen, D. O. Ferguson, J. K. Greenson, B. O. Williams, K. R. Cho, and E. R. Fearon, “Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation,” Cancer Res. 67(20), 9721–9730 (2007).
[Crossref] [PubMed]

2006 (2)

2004 (1)

J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92(5), 3121–3133 (2004).
[Crossref] [PubMed]

1998 (1)

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

1990 (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Adams, S. G.

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

Akins, M. L.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. USA 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

Aksay, E.

J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92(5), 3121–3133 (2004).
[Crossref] [PubMed]

Akyol, A.

T. Hinoi, A. Akyol, B. K. Theisen, D. O. Ferguson, J. K. Greenson, B. O. Williams, K. R. Cho, and E. R. Fearon, “Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation,” Cancer Res. 67(20), 9721–9730 (2007).
[Crossref] [PubMed]

Barretto, R. P. J.

Ben-Yakar, A.

Booth, M. J.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Botcherby, E. J.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Brown, C. M.

D. M. Huland, C. M. Brown, S. S. Howard, D. G. Ouzounov, I. Pavlova, K. Wang, D. R. Rivera, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using long gradient index lens multiphoton endoscopic systems,” Biomed. Opt. Express 3(5), 1077–1085 (2012).
[Crossref] [PubMed]

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17598–17603 (2011).
[Crossref] [PubMed]

Cho, K. R.

T. Hinoi, A. Akyol, B. K. Theisen, D. O. Ferguson, J. K. Greenson, B. O. Williams, K. R. Cho, and E. R. Fearon, “Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation,” Cancer Res. 67(20), 9721–9730 (2007).
[Crossref] [PubMed]

Clevers, H.

L. Ritsma, S. I. J. Ellenbroek, A. Zomer, H. J. Snippert, F. J. de Sauvage, B. D. Simons, H. Clevers, and J. van Rheenen, “Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging,” Nature 507(7492), 362–365 (2014).
[Crossref] [PubMed]

Cobb, M. J.

Cocker, E. D.

Cranfield, C.

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

de Sauvage, F. J.

L. Ritsma, S. I. J. Ellenbroek, A. Zomer, H. J. Snippert, F. J. de Sauvage, B. D. Simons, H. Clevers, and J. van Rheenen, “Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging,” Nature 507(7492), 362–365 (2014).
[Crossref] [PubMed]

Débarre, D.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Denk, W.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Duan, X.

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

W. Shahid, Z. Qiu, X. Duan, H. Li, T. D. Wang, and K. R. Oldham, “Modeling and Simulation of a Parametrically Resonant Micromirror With Duty-Cycled Excitation,” J. Microelectromech. Syst. 23(6), 1440–1453 (2014).
[Crossref] [PubMed]

Z. Qiu, Z. Liu, X. Duan, S. Khondee, B. Joshi, M. J. Mandella, K. Oldham, K. Kurabayashi, and T. D. Wang, “Targeted vertical cross-sectional imaging with handheld near-infrared dual axes confocal fluorescence endomicroscope,” Biomed. Opt. Express 4(2), 322–330 (2013).
[Crossref] [PubMed]

H. Li, Z. Qiu, X. Duan, K. R. Oldham, K. Kurabayashi, and T. D. Wang, “2D resonant microscanner for dual axes confocal fluorescence endomicroscope,” in Proceedings of 27th IEEE International Conference on Micro Electro Mechanical Systems (IEEE 2014), pp. 805–808.
[Crossref]

Ellenbroek, S. I. J.

L. Ritsma, S. I. J. Ellenbroek, A. Zomer, H. J. Snippert, F. J. de Sauvage, B. D. Simons, H. Clevers, and J. van Rheenen, “Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging,” Nature 507(7492), 362–365 (2014).
[Crossref] [PubMed]

Engelbrecht, C. J.

Fearon, E. R.

T. Hinoi, A. Akyol, B. K. Theisen, D. O. Ferguson, J. K. Greenson, B. O. Williams, K. R. Cho, and E. R. Fearon, “Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation,” Cancer Res. 67(20), 9721–9730 (2007).
[Crossref] [PubMed]

Ferguson, D. O.

T. Hinoi, A. Akyol, B. K. Theisen, D. O. Ferguson, J. K. Greenson, B. O. Williams, K. R. Cho, and E. R. Fearon, “Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation,” Cancer Res. 67(20), 9721–9730 (2007).
[Crossref] [PubMed]

Ferhanoglu, O.

Flusberg, B. A.

Fu, L.

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

Greenson, J. K.

T. Hinoi, A. Akyol, B. K. Theisen, D. O. Ferguson, J. K. Greenson, B. O. Williams, K. R. Cho, and E. R. Fearon, “Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation,” Cancer Res. 67(20), 9721–9730 (2007).
[Crossref] [PubMed]

Gu, M.

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

Hartwell, P. G.

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

Helmchen, F.

Hinoi, T.

T. Hinoi, A. Akyol, B. K. Theisen, D. O. Ferguson, J. K. Greenson, B. O. Williams, K. R. Cho, and E. R. Fearon, “Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation,” Cancer Res. 67(20), 9721–9730 (2007).
[Crossref] [PubMed]

Howard, S. S.

Hoy, C. L.

Huland, D. M.

Jain, A.

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

Johnston, R. S.

Joshi, B.

Joshi, B. P.

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

Jung, J. C.

J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92(5), 3121–3133 (2004).
[Crossref] [PubMed]

Juškaitis, R.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Khondee, S.

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

Z. Qiu, Z. Liu, X. Duan, S. Khondee, B. Joshi, M. J. Mandella, K. Oldham, K. Kurabayashi, and T. D. Wang, “Targeted vertical cross-sectional imaging with handheld near-infrared dual axes confocal fluorescence endomicroscope,” Biomed. Opt. Express 4(2), 322–330 (2013).
[Crossref] [PubMed]

Ko, T. H.

Kobat, D.

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17598–17603 (2011).
[Crossref] [PubMed]

Kohl, M. M.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

König, K.

Kurabayashi, K.

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

Z. Qiu, Z. Liu, X. Duan, S. Khondee, B. Joshi, M. J. Mandella, K. Oldham, K. Kurabayashi, and T. D. Wang, “Targeted vertical cross-sectional imaging with handheld near-infrared dual axes confocal fluorescence endomicroscope,” Biomed. Opt. Express 4(2), 322–330 (2013).
[Crossref] [PubMed]

H. Li, Z. Qiu, X. Duan, K. R. Oldham, K. Kurabayashi, and T. D. Wang, “2D resonant microscanner for dual axes confocal fluorescence endomicroscope,” in Proceedings of 27th IEEE International Conference on Micro Electro Mechanical Systems (IEEE 2014), pp. 805–808.
[Crossref]

Le Harzic, R.

Lee, D.

Leng, Y.

Li, H.

W. Shahid, Z. Qiu, X. Duan, H. Li, T. D. Wang, and K. R. Oldham, “Modeling and Simulation of a Parametrically Resonant Micromirror With Duty-Cycled Excitation,” J. Microelectromech. Syst. 23(6), 1440–1453 (2014).
[Crossref] [PubMed]

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

H. Li, Z. Qiu, X. Duan, K. R. Oldham, K. Kurabayashi, and T. D. Wang, “2D resonant microscanner for dual axes confocal fluorescence endomicroscope,” in Proceedings of 27th IEEE International Conference on Micro Electro Mechanical Systems (IEEE 2014), pp. 805–808.
[Crossref]

Li, M. J.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. USA 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

Li, X.

Liu, Z.

Luby-Phelps, K.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. USA 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

MacDonald, D. J.

MacDonald, N. C.

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

Mahendroo, M.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. USA 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

Mandella, M. J.

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

Z. Qiu, Z. Liu, X. Duan, S. Khondee, B. Joshi, M. J. Mandella, K. Oldham, K. Kurabayashi, and T. D. Wang, “Targeted vertical cross-sectional imaging with handheld near-infrared dual axes confocal fluorescence endomicroscope,” Biomed. Opt. Express 4(2), 322–330 (2013).
[Crossref] [PubMed]

Masedunskas, A.

A. Masedunskas, M. Sramkova, L. Parente, and R. Weigert, “Intravital Microscopy to Image Membrane Trafficking in Live Rats,” Methods Mol. Biol. 931, 153–167 (2012).
[Crossref] [PubMed]

Mehta, A. D.

J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92(5), 3121–3133 (2004).
[Crossref] [PubMed]

Messerschmidt, B.

Miller, S. A.

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

Murari, K.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. USA 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

Myaing, M. T.

Oldham, K.

Oldham, K. R.

W. Shahid, Z. Qiu, X. Duan, H. Li, T. D. Wang, and K. R. Oldham, “Modeling and Simulation of a Parametrically Resonant Micromirror With Duty-Cycled Excitation,” J. Microelectromech. Syst. 23(6), 1440–1453 (2014).
[Crossref] [PubMed]

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

H. Li, Z. Qiu, X. Duan, K. R. Oldham, K. Kurabayashi, and T. D. Wang, “2D resonant microscanner for dual axes confocal fluorescence endomicroscope,” in Proceedings of 27th IEEE International Conference on Micro Electro Mechanical Systems (IEEE 2014), pp. 805–808.
[Crossref]

Ouzounov, D. G.

D. M. Huland, C. M. Brown, S. S. Howard, D. G. Ouzounov, I. Pavlova, K. Wang, D. R. Rivera, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using long gradient index lens multiphoton endoscopic systems,” Biomed. Opt. Express 3(5), 1077–1085 (2012).
[Crossref] [PubMed]

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17598–17603 (2011).
[Crossref] [PubMed]

Owens, S. R.

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

Parente, L.

A. Masedunskas, M. Sramkova, L. Parente, and R. Weigert, “Intravital Microscopy to Image Membrane Trafficking in Live Rats,” Methods Mol. Biol. 931, 153–167 (2012).
[Crossref] [PubMed]

Paulsen, O.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Pavlova, I.

D. M. Huland, C. M. Brown, S. S. Howard, D. G. Ouzounov, I. Pavlova, K. Wang, D. R. Rivera, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using long gradient index lens multiphoton endoscopic systems,” Biomed. Opt. Express 3(5), 1077–1085 (2012).
[Crossref] [PubMed]

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17598–17603 (2011).
[Crossref] [PubMed]

Piyawattanametha, W.

Qiu, Z.

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

W. Shahid, Z. Qiu, X. Duan, H. Li, T. D. Wang, and K. R. Oldham, “Modeling and Simulation of a Parametrically Resonant Micromirror With Duty-Cycled Excitation,” J. Microelectromech. Syst. 23(6), 1440–1453 (2014).
[Crossref] [PubMed]

Z. Qiu, Z. Liu, X. Duan, S. Khondee, B. Joshi, M. J. Mandella, K. Oldham, K. Kurabayashi, and T. D. Wang, “Targeted vertical cross-sectional imaging with handheld near-infrared dual axes confocal fluorescence endomicroscope,” Biomed. Opt. Express 4(2), 322–330 (2013).
[Crossref] [PubMed]

H. Li, Z. Qiu, X. Duan, K. R. Oldham, K. Kurabayashi, and T. D. Wang, “2D resonant microscanner for dual axes confocal fluorescence endomicroscope,” in Proceedings of 27th IEEE International Conference on Micro Electro Mechanical Systems (IEEE 2014), pp. 805–808.
[Crossref]

Ra, H.

Riemann, I.

Ritsma, L.

L. Ritsma, S. I. J. Ellenbroek, A. Zomer, H. J. Snippert, F. J. de Sauvage, B. D. Simons, H. Clevers, and J. van Rheenen, “Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging,” Nature 507(7492), 362–365 (2014).
[Crossref] [PubMed]

Rivera, D. R.

D. M. Huland, C. M. Brown, S. S. Howard, D. G. Ouzounov, I. Pavlova, K. Wang, D. R. Rivera, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using long gradient index lens multiphoton endoscopic systems,” Biomed. Opt. Express 3(5), 1077–1085 (2012).
[Crossref] [PubMed]

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17598–17603 (2011).
[Crossref] [PubMed]

Schnitzer, M. J.

Seibel, E. J.

Shahid, W.

W. Shahid, Z. Qiu, X. Duan, H. Li, T. D. Wang, and K. R. Oldham, “Modeling and Simulation of a Parametrically Resonant Micromirror With Duty-Cycled Excitation,” J. Microelectromech. Syst. 23(6), 1440–1453 (2014).
[Crossref] [PubMed]

Simons, B. D.

L. Ritsma, S. I. J. Ellenbroek, A. Zomer, H. J. Snippert, F. J. de Sauvage, B. D. Simons, H. Clevers, and J. van Rheenen, “Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging,” Nature 507(7492), 362–365 (2014).
[Crossref] [PubMed]

Smith, C. W.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Snippert, H. J.

L. Ritsma, S. I. J. Ellenbroek, A. Zomer, H. J. Snippert, F. J. de Sauvage, B. D. Simons, H. Clevers, and J. van Rheenen, “Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging,” Nature 507(7492), 362–365 (2014).
[Crossref] [PubMed]

Solgaard, O.

Sramkova, M.

A. Masedunskas, M. Sramkova, L. Parente, and R. Weigert, “Intravital Microscopy to Image Membrane Trafficking in Live Rats,” Methods Mol. Biol. 931, 153–167 (2012).
[Crossref] [PubMed]

Stepnoski, R.

J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92(5), 3121–3133 (2004).
[Crossref] [PubMed]

Strickler, J. H.

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Strogatz, S. H.

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

Theisen, B. K.

T. Hinoi, A. Akyol, B. K. Theisen, D. O. Ferguson, J. K. Greenson, B. O. Williams, K. R. Cho, and E. R. Fearon, “Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation,” Cancer Res. 67(20), 9721–9730 (2007).
[Crossref] [PubMed]

Turner, K. L.

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

van Rheenen, J.

L. Ritsma, S. I. J. Ellenbroek, A. Zomer, H. J. Snippert, F. J. de Sauvage, B. D. Simons, H. Clevers, and J. van Rheenen, “Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging,” Nature 507(7492), 362–365 (2014).
[Crossref] [PubMed]

Wang, K.

Wang, T. D.

W. Shahid, Z. Qiu, X. Duan, H. Li, T. D. Wang, and K. R. Oldham, “Modeling and Simulation of a Parametrically Resonant Micromirror With Duty-Cycled Excitation,” J. Microelectromech. Syst. 23(6), 1440–1453 (2014).
[Crossref] [PubMed]

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

Z. Qiu, Z. Liu, X. Duan, S. Khondee, B. Joshi, M. J. Mandella, K. Oldham, K. Kurabayashi, and T. D. Wang, “Targeted vertical cross-sectional imaging with handheld near-infrared dual axes confocal fluorescence endomicroscope,” Biomed. Opt. Express 4(2), 322–330 (2013).
[Crossref] [PubMed]

H. Li, Z. Qiu, X. Duan, K. R. Oldham, K. Kurabayashi, and T. D. Wang, “2D resonant microscanner for dual axes confocal fluorescence endomicroscope,” in Proceedings of 27th IEEE International Conference on Micro Electro Mechanical Systems (IEEE 2014), pp. 805–808.
[Crossref]

Webb, W. W.

D. M. Huland, C. M. Brown, S. S. Howard, D. G. Ouzounov, I. Pavlova, K. Wang, D. R. Rivera, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using long gradient index lens multiphoton endoscopic systems,” Biomed. Opt. Express 3(5), 1077–1085 (2012).
[Crossref] [PubMed]

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17598–17603 (2011).
[Crossref] [PubMed]

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Weigert, R.

A. Masedunskas, M. Sramkova, L. Parente, and R. Weigert, “Intravital Microscopy to Image Membrane Trafficking in Live Rats,” Methods Mol. Biol. 931, 153–167 (2012).
[Crossref] [PubMed]

Weinigel, M.

Williams, B. O.

T. Hinoi, A. Akyol, B. K. Theisen, D. O. Ferguson, J. K. Greenson, B. O. Williams, K. R. Cho, and E. R. Fearon, “Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation,” Cancer Res. 67(20), 9721–9730 (2007).
[Crossref] [PubMed]

Wilson, T.

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Wu, Y.

Xi, J.

Xie, H.

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

Xu, C.

D. M. Huland, C. M. Brown, S. S. Howard, D. G. Ouzounov, I. Pavlova, K. Wang, D. R. Rivera, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using long gradient index lens multiphoton endoscopic systems,” Biomed. Opt. Express 3(5), 1077–1085 (2012).
[Crossref] [PubMed]

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17598–17603 (2011).
[Crossref] [PubMed]

Yildirim, M.

Zhang, Y.

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. USA 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

Zhou, Q.

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

Zomer, A.

L. Ritsma, S. I. J. Ellenbroek, A. Zomer, H. J. Snippert, F. J. de Sauvage, B. D. Simons, H. Clevers, and J. van Rheenen, “Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging,” Nature 507(7492), 362–365 (2014).
[Crossref] [PubMed]

Appl. Opt. (1)

Biomed. Opt. Express (2)

Cancer Res. (1)

T. Hinoi, A. Akyol, B. K. Theisen, D. O. Ferguson, J. K. Greenson, B. O. Williams, K. R. Cho, and E. R. Fearon, “Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation,” Cancer Res. 67(20), 9721–9730 (2007).
[Crossref] [PubMed]

Gastroenterology (1)

Z. Qiu, S. Khondee, X. Duan, H. Li, M. J. Mandella, B. P. Joshi, Q. Zhou, S. R. Owens, K. Kurabayashi, K. R. Oldham, and T. D. Wang, “Vertical Cross-Sectional Imaging of Colonic Dysplasia In Vivo With Multi-spectral Dual Axes Confocal Endomicroscopy,” Gastroenterology 146(3), 615–617 (2014).
[Crossref] [PubMed]

J. Biomed. Opt. (1)

L. Fu, A. Jain, C. Cranfield, H. Xie, and M. Gu, “Three-dimensional nonlinear optical endoscopy,” J. Biomed. Opt. 12(4), 040501 (2007).
[Crossref] [PubMed]

J. Microelectromech. Syst. (1)

W. Shahid, Z. Qiu, X. Duan, H. Li, T. D. Wang, and K. R. Oldham, “Modeling and Simulation of a Parametrically Resonant Micromirror With Duty-Cycled Excitation,” J. Microelectromech. Syst. 23(6), 1440–1453 (2014).
[Crossref] [PubMed]

J. Neurophysiol. (1)

J. C. Jung, A. D. Mehta, E. Aksay, R. Stepnoski, and M. J. Schnitzer, “In vivo mammalian brain imaging using one- and two-photon fluorescence microendoscopy,” J. Neurophysiol. 92(5), 3121–3133 (2004).
[Crossref] [PubMed]

Methods Mol. Biol. (1)

A. Masedunskas, M. Sramkova, L. Parente, and R. Weigert, “Intravital Microscopy to Image Membrane Trafficking in Live Rats,” Methods Mol. Biol. 931, 153–167 (2012).
[Crossref] [PubMed]

Nature (2)

K. L. Turner, S. A. Miller, P. G. Hartwell, N. C. MacDonald, S. H. Strogatz, and S. G. Adams, “Five parametric resonances in a microelectromechanical system,” Nature 396(6707), 149–152 (1998).
[Crossref]

L. Ritsma, S. I. J. Ellenbroek, A. Zomer, H. J. Snippert, F. J. de Sauvage, B. D. Simons, H. Clevers, and J. van Rheenen, “Intestinal crypt homeostasis revealed at single-stem-cell level by in vivo live imaging,” Nature 507(7492), 362–365 (2014).
[Crossref] [PubMed]

Opt. Express (3)

Opt. Lett. (3)

Proc. Natl. Acad. Sci. U.S.A. (1)

D. R. Rivera, C. M. Brown, D. G. Ouzounov, I. Pavlova, D. Kobat, W. W. Webb, and C. Xu, “Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue,” Proc. Natl. Acad. Sci. U.S.A. 108(43), 17598–17603 (2011).
[Crossref] [PubMed]

Proc. Natl. Acad. Sci. USA (2)

Y. Zhang, M. L. Akins, K. Murari, J. Xi, M. J. Li, K. Luby-Phelps, M. Mahendroo, and X. Li, “A compact fiber-optic SHG scanning endomicroscope and its application to visualize cervical remodeling during pregnancy,” Proc. Natl. Acad. Sci. USA 109(32), 12878–12883 (2012).
[Crossref] [PubMed]

E. J. Botcherby, C. W. Smith, M. M. Kohl, D. Débarre, M. J. Booth, R. Juškaitis, O. Paulsen, and T. Wilson, “Aberration-free three-dimensional multiphoton imaging of neuronal activity at kHz rates,” Proc. Natl. Acad. Sci. USA 109(8), 2919–2924 (2012).
[Crossref] [PubMed]

Science (1)

W. Denk, J. H. Strickler, and W. W. Webb, “Two-photon laser scanning fluorescence microscopy,” Science 248(4951), 73–76 (1990).
[Crossref] [PubMed]

Other (1)

H. Li, Z. Qiu, X. Duan, K. R. Oldham, K. Kurabayashi, and T. D. Wang, “2D resonant microscanner for dual axes confocal fluorescence endomicroscope,” in Proceedings of 27th IEEE International Conference on Micro Electro Mechanical Systems (IEEE 2014), pp. 805–808.
[Crossref]

Supplementary Material (2)

NameDescription
» Visualization 1: MPG (13662 KB)      Normal colon
» Visualization 2: MPG (13662 KB)      Dysplastic colon

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Figures (6)

Fig. 1
Fig. 1 Schematic. Handheld multiphoton endomicroscope shown in dashed box. Details provided in text.
Fig. 2
Fig. 2 Zemax Simulation. a) Ray-trace simulation for design of the distal optics (L3-L6). A field-of-view (FOV) of 300 × 300 μm2 can be achieved with a lateral mechanical scan angle of ± 4.5°. b), c), d) Spot size (RMS radius) of 0.33, 1.265 and 2.168 μm can be achieved at a distance of 0, 70 and 150 μm away from the center of the FOV.
Fig. 3
Fig. 3 MEMS scanner. a) Schematic shows dimensions of the 2D MEMS scanner. b) SEM of fabricated scanner. Frequency response for upsweep and downsweep to drive scanner in the c) X and d) Y axes at the fundamental drive frequencies where n = 1.
Fig. 4
Fig. 4 Endomicroscope packaging. a) CAD drawing. b) Distal focusing optics. c) Handheld instrument can be used to perform repetitive imaging in small animal models of human disease. d) MEMS scanner.
Fig. 5
Fig. 5 Image resolution. a) Reflectance image of standard target (USAF 1951). Fluorescence intensity profiles of 100 nm beads show full-width at half maximum (FWHM) of b) 2.03 μm in lateral and c) 9.02 μm in axial directions.
Fig. 6
Fig. 6 Imaging results. a) Single frame from multiphoton excited fluorescence video (Visualization 1) of normal colonic mucosa collected in vivo at 5 frames/sec. b) Ex vivo image from normal averaged over 5 frames. c) Corresponding histology (H&E) of normal colon. Single frame from video of dysplastic crypts from colon of CPC;Apc mouse collected d) in vivo (Visualization 2) at 5 frames/sec and e) ex vivo (averaged over 5 frames). f) Corresponding histology (H&E) of dysplasia.

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