Abstract

Three-dimensional cellular imaging techniques have become indispensable tools in biological research and medical diagnostics. Conventional 3D imaging approaches employ focal stack collection to image different planes of the cell. In this work, we present the design and fabrication of a slanted channel microfluidic chip for 3D fluorescence imaging of cells in flow. The approach employs slanted microfluidic channels fabricated in glass using ultrafast laser inscription. The slanted nature of the microfluidic channels ensures that samples come into and go out of focus, as they pass through the microscope imaging field of view. This novel approach enables the collection of focal stacks in a straight-forward and automated manner, even with off-the-shelf microscopes that are not equipped with any motorized translation/rotation sample stages. The presented approach not only simplifies conventional focal stack collection, but also enhances the capabilities of a regular widefield fluorescence microscope to match the features of a sophisticated confocal microscope. We demonstrate the retrieval of sectioned slices of microspheres and cells, with the use of computational algorithms to enhance the signal-to-noise ratio (SNR) in the collected raw images. The retrieved sectioned images have been used to visualize fluorescent microspheres and bovine sperm cell nucleus in 3D while using a regular widefield fluorescence microscope. We have been able to achieve sectioning of approximately 200 slices per cell, which corresponds to a spatial translation of ∼ 15 nm per slice along the optical axis of the microscope.

Published by The Optical Society under the terms of the Creative Commons Attribution 4.0 License. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

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References

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2016 (1)

V. K. Jagannadh, B. P. Bhat, L. A. N. Julius, and S. S. Gorthi, “High-throughput miniaturized microfluidic microscopy with radially parallelized channel geometry,” Anal Bioanal Chem 408, 1909–1916 (2016).
[Crossref] [PubMed]

2015 (5)

M. Haifler, P. Girshovitz, G. Band, G. Dardikman, I. Madjar, and N. T. Shaked, “Interferometric phase microscopy for label-free morphological evaluation of sperm cells,” Fertil. and Steril. 104, 43–47 (2015).
[Crossref]

V. K. Jagannadh, M. D. Mackenzie, P. Pal, A. K. Kar, and S. S. Gorthi, “Imaging Flow Cytometry With Femtosecond Laser-Micromachined Glass Microfluidic Channels,” IEEE J of Sel. Topics in Quantum Electron. 21, 370–375 (2015).
[Crossref]

G. Di Caprio, M. A. Ferrara, L. Miccio, F. Merola, P. Memmolo, P. Ferraro, and G. Coppola, “Holographic imaging of unlabelled sperm cells for semen analysis: a review,” J Biophotonics 8, 779–789 (2015).
[Crossref]

M. A. Ferrara, G. Di Caprio, S. Managó, A. De Angelis, L. Sirleto, G. Coppola, and A. C. De Luca, “Label-free imaging and biochemical characterization of bovine sperm cells,” Biosensors (Basel) 5, 141–157 (2015).
[Crossref]

M. Saxena, G. Eluru, and S. S. Gorthi, “Structured illumination microscopy,” Adv. Opt. Photon. 7, 241–275 (2015).
[Crossref]

2014 (8)

M. Beresna, M. Gecevicȗius, and P. G. Kazansky, “Ultrafast laser direct writing and nanostructuring in transparent materials,” Adv. Opt. Photon. 6, 293 (2014).
[Crossref]

Y. Sung, N. Lue, B. Hamza, J. Martel, D. Irimia, R. R. Dasari, W. Choi, Z. Yaqoob, and P. So, “Three-dimensional holographic refractive-index measurement of continuously flowing cells in a microfluidic channel,” Phys. Rev. Applied 1, 014002 (2014).
[Crossref]

G. M. Church, M. B. Elowitz, C. D. Smolke, C. A. Voigt, and R. Weiss, “Realizing the potential of synthetic biology,” Nat Rev Mol Cell Biol 15, 289–294 (2014).
[Crossref] [PubMed]

K. Sugioka and Y. Cheng, “Ultrafast lasers-reliable tools for advanced materials processing,” Light Sci Appl 3, e149 (2014).
[Crossref]

F. He, Y. Liao, J. Lin, J. Song, L. Qiao, Y. Cheng, and K. Sugioka, “Femtosecond Laser Fabrication of Monolithically Integrated Microfluidic Sensors in Glass,” Sensors 14, 19402–19440 (2014).
[Crossref] [PubMed]

P. Paié, F. Bragheri, R. M. Vazquez, and R. Osellame, “Straightforward 3d hydrodynamic focusing in femtosecond laser fabricated microfluidic channels,” Lab Chip 14, 1826–1833 (2014).
[Crossref] [PubMed]

E. J. van Beers, L. Samsel, L. Mendelsohn, R. Saiyed, K. Y. Fertrin, C. A. Brantner, M. P. Daniels, J. Nichols, J. P. McCoy, and G. J. Kato, “Imaging flow cytometry for automated detection of hypoxia-induced erythrocyte shape change in sickle cell disease,” Am. J. Hematol. 89, 598–603 (2014).
[Crossref] [PubMed]

L. M. Niswander, K. E. McGrath, J. C. Kennedy, and J. Palis, “Improved quantitative analysis of primary bone marrow megakaryocytes utilizing imaging flow cytometry,” Cytometry A 85, 302–312 (2014).
[Crossref] [PubMed]

2013 (3)

B.-B. Xu, Y.-L. Zhang, H. Xia, W.-F. Dong, H. Ding, and H.-B. Sun, “Fabrication and multifunction integration of microfluidic chips by femtosecond laser direct writing,” Lab Chip 13, 1677–1690 (2013).
[Crossref] [PubMed]

J. Wu, J. Li, and R. K. Y. Chan, “A light sheet based high throughput 3d-imaging flow cytometer for phytoplankton analysis,” Opt. Express 21, 14474–14480 (2013).
[Crossref] [PubMed]

N. C. Pégard and J. W. Fleischer, “Three-dimensional deconvolution microfluidic microscopy using a tilted channel,” J. Biomed. Opt 18, 040503 (2013).
[Crossref] [PubMed]

2012 (6)

S. S. Gorthi and E. Schonbrun, “Phase imaging flow cytometry using a focus-stack collecting microscope,” Opt. Lett. 37, 707–709 (2012).
[Crossref] [PubMed]

D. Choudhury, D. Jaque, A. Rodenas, W. T. Ramsay, L. Paterson, and A. K. Kar, “Quantum dot enabled thermal imaging of optofluidic devices,” Lab Chip 12, 2414–2420 (2012).
[Crossref] [PubMed]

D. Choudhury, W. T. Ramsay, R. Kiss, N. A. Willoughby, L. Paterson, and A. K. Kar, “A 3d mammalian cell separator biochip,” Lab Chip 12, 948 (2012).
[Crossref] [PubMed]

N. G. Cassuto, A. Hazout, I. Hammoud, R. Balet, D. Bouret, Y. Barak, S. Jellad, J. M. Plouchart, J. Selva, and C. Yazbeck, “Correlation between DNA defect and sperm-head morphology,” Reprod. Biomed. Online 24, 211–218 (2012).
[Crossref] [PubMed]

K. Goda, A. Ayazi, D. R. Gossett, J. Sadasivam, C. K. Lonappan, E. Sollier, A. M. Fard, S. C. Hur, J. Adam, C. Murray, C. Wang, N. Brackbill, D. D. Carlo, and B. Jalali, “High-throughput single-microparticle imaging flow analyzer,” PNAS 109, 11630–11635 (2012).
[Crossref] [PubMed]

E. Schonbrun, S. S. Gorthi, and D. Schaak, “Microfabricated multiple field of view imaging flow cytometry,” Lab Chip 12, 268–273 (2012).
[Crossref]

2011 (3)

J. Mertz, “Optical sectioning microscopy with planar or structured illumination,” Nat Meth 8, 811–819 (2011).
[Crossref]

L. Shao, P. Kner, E. H. Rego, and M. G. L. Gustafsson, “Super-resolution 3d microscopy of live whole cells using structured illumination,” Nat Meth 8, 1044–1046 (2011).
[Crossref]

P. Memmolo, G. Di Caprio, C. Distante, M. Paturzo, R. Puglisi, D. Balduzzi, A. Galli, G. Coppola, and P. ao, “Identification of bovine sperm head for morphometry analysis in quantitative phase-contrast holographic microscopy,” Opt Express 19, 23215–23226 (2011).
[Crossref] [PubMed]

2010 (1)

T. G. Cooper, E. Noonan, S. von Eckardstein, J. Auger, H. W. G. Baker, H. M. Behre, T. B. Haugen, T. Kruger, C. Wang, M. T. Mbizvo, and K. M. Vogelsong, “World Health Organization reference values for human semen characteristics,” Hum. Reprod. Update 16, 231–245 (2010).
[Crossref]

2008 (1)

S. M. Rafelski and W. F. Marshall, “Building the cell: design principles of cellular architecture,” Nat Rev Mol Cell Biol 9, 593–602 (2008).
[Crossref] [PubMed]

2007 (1)

D. A. Basiji, W. E. Ortyn, L. Liang, V. Venkatachalam, and P. Morrissey, “Cellular Image Analysis and Imaging by Flow Cytometry,” Clinics in laboratory medicine 27, 653–658 (2007).
[Crossref] [PubMed]

2006 (2)

P. Sarder and A. Nehorai, “Deconvolution methods for 3-D fluorescence microscopy images,” IEEE Signal Processing Magazine 23, 32–45 (2006).
[Crossref]

X. Heng, D. Erickson, L. R. Baugh, Z. Yaqoob, P. W. Sternberg, D. Psaltis, and C. Yang, “Optofluidic microscopy-a method for implementing a high resolution optical microscope on a chip,” Lab Chip 6, 1274–1276 (2006).
[Crossref] [PubMed]

2004 (1)

D. Zink, A. H. Fischer, and J. A. Nickerson, “Nuclear structure in cancer cells,” Nat Rev Cancer 4, 677–687 (2004).
[Crossref] [PubMed]

2002 (1)

2001 (1)

J. C. Love, J. R. Anderson, and G. M. Whitesides, “Fabrication of Three-Dimensional Microfluidic Systems by Soft Lithography,” MRS Bulletin 26, 523–528 (2001).
[Crossref]

1998 (1)

Y. Xia and G. M. Whitesides, “Soft lithography,” Ann. Rev. of Mater. Sci. 28, 153–184 (1998).
[Crossref]

1985 (1)

G. J. Brakenhoff, H. T. M. van der Voort, E. A. van Spronsen, W. a. M. Linnemans, and N. Nanninga, “Three-dimensional chromatin distribution in neuroblastoma nuclei shown by confocal scanning laser microscopy,” Nature 317, 748–749 (1985).
[Crossref] [PubMed]

Adam, J.

K. Goda, A. Ayazi, D. R. Gossett, J. Sadasivam, C. K. Lonappan, E. Sollier, A. M. Fard, S. C. Hur, J. Adam, C. Murray, C. Wang, N. Brackbill, D. D. Carlo, and B. Jalali, “High-throughput single-microparticle imaging flow analyzer,” PNAS 109, 11630–11635 (2012).
[Crossref] [PubMed]

Alberts, B.

B. Alberts, D. Bray, K. Hopkin, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, Essential Cell Biology, 4 Edition (Garland Science, 2013).

Anderson, J. R.

J. C. Love, J. R. Anderson, and G. M. Whitesides, “Fabrication of Three-Dimensional Microfluidic Systems by Soft Lithography,” MRS Bulletin 26, 523–528 (2001).
[Crossref]

ao, P.

P. Memmolo, G. Di Caprio, C. Distante, M. Paturzo, R. Puglisi, D. Balduzzi, A. Galli, G. Coppola, and P. ao, “Identification of bovine sperm head for morphometry analysis in quantitative phase-contrast holographic microscopy,” Opt Express 19, 23215–23226 (2011).
[Crossref] [PubMed]

Auger, J.

T. G. Cooper, E. Noonan, S. von Eckardstein, J. Auger, H. W. G. Baker, H. M. Behre, T. B. Haugen, T. Kruger, C. Wang, M. T. Mbizvo, and K. M. Vogelsong, “World Health Organization reference values for human semen characteristics,” Hum. Reprod. Update 16, 231–245 (2010).
[Crossref]

Ayazi, A.

K. Goda, A. Ayazi, D. R. Gossett, J. Sadasivam, C. K. Lonappan, E. Sollier, A. M. Fard, S. C. Hur, J. Adam, C. Murray, C. Wang, N. Brackbill, D. D. Carlo, and B. Jalali, “High-throughput single-microparticle imaging flow analyzer,” PNAS 109, 11630–11635 (2012).
[Crossref] [PubMed]

Baker, H. W. G.

T. G. Cooper, E. Noonan, S. von Eckardstein, J. Auger, H. W. G. Baker, H. M. Behre, T. B. Haugen, T. Kruger, C. Wang, M. T. Mbizvo, and K. M. Vogelsong, “World Health Organization reference values for human semen characteristics,” Hum. Reprod. Update 16, 231–245 (2010).
[Crossref]

Balduzzi, D.

P. Memmolo, G. Di Caprio, C. Distante, M. Paturzo, R. Puglisi, D. Balduzzi, A. Galli, G. Coppola, and P. ao, “Identification of bovine sperm head for morphometry analysis in quantitative phase-contrast holographic microscopy,” Opt Express 19, 23215–23226 (2011).
[Crossref] [PubMed]

Balet, R.

N. G. Cassuto, A. Hazout, I. Hammoud, R. Balet, D. Bouret, Y. Barak, S. Jellad, J. M. Plouchart, J. Selva, and C. Yazbeck, “Correlation between DNA defect and sperm-head morphology,” Reprod. Biomed. Online 24, 211–218 (2012).
[Crossref] [PubMed]

Band, G.

M. Haifler, P. Girshovitz, G. Band, G. Dardikman, I. Madjar, and N. T. Shaked, “Interferometric phase microscopy for label-free morphological evaluation of sperm cells,” Fertil. and Steril. 104, 43–47 (2015).
[Crossref]

Barak, Y.

N. G. Cassuto, A. Hazout, I. Hammoud, R. Balet, D. Bouret, Y. Barak, S. Jellad, J. M. Plouchart, J. Selva, and C. Yazbeck, “Correlation between DNA defect and sperm-head morphology,” Reprod. Biomed. Online 24, 211–218 (2012).
[Crossref] [PubMed]

Basiji, D. A.

D. A. Basiji, W. E. Ortyn, L. Liang, V. Venkatachalam, and P. Morrissey, “Cellular Image Analysis and Imaging by Flow Cytometry,” Clinics in laboratory medicine 27, 653–658 (2007).
[Crossref] [PubMed]

Bassi, A.

P. Paié, F. Bragheri, A. Bassi, and R. Osellame, “Selective plane illumination microscopy on a chip,” Lab Chip (2016).
[Crossref] [PubMed]

Baugh, L. R.

X. Heng, D. Erickson, L. R. Baugh, Z. Yaqoob, P. W. Sternberg, D. Psaltis, and C. Yang, “Optofluidic microscopy-a method for implementing a high resolution optical microscope on a chip,” Lab Chip 6, 1274–1276 (2006).
[Crossref] [PubMed]

Behre, H. M.

T. G. Cooper, E. Noonan, S. von Eckardstein, J. Auger, H. W. G. Baker, H. M. Behre, T. B. Haugen, T. Kruger, C. Wang, M. T. Mbizvo, and K. M. Vogelsong, “World Health Organization reference values for human semen characteristics,” Hum. Reprod. Update 16, 231–245 (2010).
[Crossref]

Beresna, M.

Bhaduri, B.

M. Mir, B. Bhaduri, R. Wang, R. Zhu, and G. Popescu, “Chapter 3 - Quantitative Phase Imaging,” in “Progress in Optics,”, vol. 57 of Progress in Optics E. Wolf, ed. (Elsevier, 2012), pp. 133–217.
[Crossref]

Bhat, B. P.

V. K. Jagannadh, B. P. Bhat, L. A. N. Julius, and S. S. Gorthi, “High-throughput miniaturized microfluidic microscopy with radially parallelized channel geometry,” Anal Bioanal Chem 408, 1909–1916 (2016).
[Crossref] [PubMed]

Bouret, D.

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B.-B. Xu, Y.-L. Zhang, H. Xia, W.-F. Dong, H. Ding, and H.-B. Sun, “Fabrication and multifunction integration of microfluidic chips by femtosecond laser direct writing,” Lab Chip 13, 1677–1690 (2013).
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Figures (10)

Fig. 1
Fig. 1

(a) Schematic Design of the Proposed ULI based Universal Focal Stack Collection Device. (b) Schematic representation of motion of the cell through the focal stack collection device within the microscope FOV.

Fig. 2
Fig. 2

Images of focal stack collection glass microfluidic device after etching. (a) Microscopic Top view of the device (b) Microscopic side view of a device having channels with a 1 degree tilt. (c) Microscopic side view of a device having channels with 5 degree tilt. (d) Top view of the device displaying it’s lateral width. (e) Side of the device, showing it’s thickness.

Fig. 3
Fig. 3

S1. (a) Conventional wide-field fluorescence microscope fitted with digital camera. (b) Zoomed in view of the sample stage, showing the flat-mounted focus stack collecting microfluidic device.

Fig. 4
Fig. 4

(a) Raw, (b) Deconvolved Focal stack of a 4 μm fluorescent microsphere. (c) Slices of fluorescent microsphere, after removal of artifacts. Length of Scale bar is 10 μm.

Fig. 5
Fig. 5

Intensity Profiles drawn across the surface of two different slices of the fluorescent bead. (a) Image of the edge slice, the intensity profile shown is over the line across image. (b) Image of the Center slice, the intensity profile shown is over the line across image.

Fig. 6
Fig. 6

Comparison of photon reassignment, when different number of slices are used for deconvolution. The intensity profiles across the restored images when (a) Full stack (44 slices), (b) 22 slices, (c) 15 slices were used for reconstruction. The (d) raw image of the same plane and it’s corresponding intensity profile have been shown. Length of scale bar is 10 μm.

Fig. 7
Fig. 7

3D visualization of the 4 μm fluorescent microsphere.

Fig. 8
Fig. 8

Histogram for the size of fluorescent microspheres as measured using the presented slanted channel microfluidic chip.

Fig. 9
Fig. 9

(a) Raw focal stack of Bovine sperm cell nucleus. (b) Deconvolved focal stack of Bovine sperm cell nucleus. (c) Slices of bovine sperm cell nucleus, after removal of artifacts. Length of scale bar is 10 μm.

Fig. 10
Fig. 10

3D visualization of Bovine Sperm Cell nucleus.

Equations (2)

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d = l × tan ( θ )
θ arctan ( 2 × s l )

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