Abstract

In this work we demonstrate, to the best of our knowledge, a novel wide field-of-view upconversion system, supporting upconversion of monochromatic mid-infrared (mid-IR) images, e.g., for hyperspectral imaging (HSI). An optical parametric oscillator delivering 20 ps pulses tunable in the 2.3–4 μm range acts as a monochromatic mid-IR illumination source. A standard CCD camera, in synchronism with the crystal rotation of the upconversion system, acquires in only 2.5 ms the upconverted mid-IR images containing 64 kpixels, thereby eliminating the need for postprocessing. This approach is generic in nature and constitutes a major simplification in realizing video-frame-rate mid-IR monochromatic imaging. A second part of this paper includes a proof-of-principle study on esophageal tissues samples, from a tissue microarray, in the 3–4 μm wavelength range. The use of mid-IR HSI for investigation of esophageal cancers is particularly promising as it allows for a much faster and possibly more observer-independent workflow than state-of-the-art histology. Comparing histologically stained sections evaluated by a pathologist to images obtained by either Fourier transform IR or upconversion HSI based on machine learning shows great promise for further work pointing towards clinical translation using the presented mid-IR HSI upconversion system.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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    [Crossref]

2018 (6)

S. Mittal, K. L. S. Yeh Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

C. Kuepper, A. Kallenbach-Thieltges, H. Juette, A. Tannapfel, F. Großerueschkamp, and K. Gerwert, “Quantum cascade laser based infrared microscopy for label-free and automated cancer classification in tissue sections,” Sci. Rep. 8, 7717 (2018).
[Crossref]

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

S. Mittal, K. Yeh, L. S. Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

S. Junaid, J. Tomko, W. T. Masselink, C. Pedersen, and P. Tidemand-Lichtenberg, “Mid-infrared upconversion based hyperspectral imaging,” Opt. Express 26, 2203–2211 (2018).
[Crossref]

R. Demur, R. Graioud, A. Grisard, E. Lallier, L. Leviandier, L. Morvan, N. Treps, and C. Fabre, “Near-infrared to visible upconversion imaging using a broadband pump laser,” Opt. Express 26, 13252–13263 (2018).
[Crossref]

2017 (3)

M. Mathez, P. J. Rodrigo, P. Tidemand-Lichtenberg, and C. Pedersen, “Upconversion imaging using short-wave infrared picosecond pulses,” Opt. Lett. 42, 579–582 (2017).
[Crossref]

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

M. J. Pilling, A. Henderson, J. H. Shanks, M. D. Brown, N. W. Clarke, and P. Gardner, “Infrared spectral histopathology using haematoxylin and eosin (H&E) stained glass slides: a major step forward towards clinical translation,” Analyst 142, 1258–1268 (2017).
[Crossref]

2016 (1)

J. Nallala, G. R. Lloyd, M. Hermes, N. Shepherd, and N. Stone, “Enhanced spectral histology in the colon using high-magnification benchtop FTIR imaging,” Vib. Spectrosc. 91, 83–91 (2016).
[Crossref]

2015 (4)

2014 (2)

L. Høgstedt, J. S. Dam, A.-L. Sahlberg, Z. Li, M. Aldén, C. Pedersen, and P. Tidemand-Lichtenberg, “Low-noise mid-IR upconversion detector for improved IR-degenerate four-wave mixing gas sensing,” Opt. Lett. 39, 5321–5324 (2014).
[Crossref]

M. Ebrahim-Zadeh and S. Chaitanya Kumar, “Yb-fiber-laser-pumped ultrafast frequency conversion sources from the mid-Infrared to the ultraviolet,” IEEE J. Sel. Top. Quantum Electron. 20, 7600519 (2014).
[Crossref]

2012 (6)

2010 (2)

A. Travo, O. Piot, R. Wolthuis, C. Gobinet, M. Manfait, J. Bara, M. E. Forgue-Lafitte, and P. Jeanneson, “IR spectral imaging of secreted mucus: a promising new tool for the histopathological recognition of human colonic adenocarcinomas,” Histopathology 56, 921–931 (2010).
[Crossref]

M. N. Abedin, M. G. Mlynczak, and T. F. Refaat, “Infrared detectors overview in the short-wave infrared to far-infrared for CLARREO mission,” Proc. SPIE 7808, 780801 (2010).
[Crossref]

2005 (2)

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol. 23, 469–474 (2005).
[Crossref]

J. Houghton, “Global warming,” Rep. Prog. Phys. 68, 1343–1403(2005).
[Crossref]

2002 (1)

A. Rogalski, “Infrared detectors: an overview,” Infrared Phys. Technol. 43, 187–210 (2002).
[Crossref]

1992 (1)

M. J. T. Milton, T. J. McIlveen, D. C. Hanna, and P. T. Woods, “High-efficiency infrared generation by difference-frequency mixing using tangential phase matching,” Opt. Commun. 87, 273–277 (1992).
[Crossref]

1979 (1)

J. A. Hartigan and M. A. Wong, “A K-means clustering algorithm,” Appl. Statist. 28, 100–108 (1979).
[Crossref]

1969 (2)

J. Warner, “Phase-matching for optical up-conversion with maximum angular aperture—theory and practice,” Opto-Electronics 1, 25–28 (1969).
[Crossref]

R. A. Andrews, “Wide angular aperture image upconversion,” IEEE J. Quantum Electron. 5, 548–550 (1969).
[Crossref]

Abedin, M. N.

M. N. Abedin, M. G. Mlynczak, and T. F. Refaat, “Infrared detectors overview in the short-wave infrared to far-infrared for CLARREO mission,” Proc. SPIE 7808, 780801 (2010).
[Crossref]

Aldén, M.

Almond, M.

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

Amrania, H.

Andrews, R. A.

R. A. Andrews, “Wide angular aperture image upconversion,” IEEE J. Quantum Electron. 5, 548–550 (1969).
[Crossref]

Antonacci, G.

Bakker, W. H.

D. F. Meer, H. M. A. Werff, F. J. A. Ruitenbeek, C. A. Hecker, W. H. Bakker, M. F. Noomen, M. Meijde, E. J. M. Carranza, J. B. Smeth, and T. Woldai, “Multi and hyperspectral geologic remote sensing: A review,” Int. J. Appl. Earth Obs. Geinf. 14, 112–128 (2012).
[Crossref]

Bara, J.

A. Travo, O. Piot, R. Wolthuis, C. Gobinet, M. Manfait, J. Bara, M. E. Forgue-Lafitte, and P. Jeanneson, “IR spectral imaging of secreted mucus: a promising new tool for the histopathological recognition of human colonic adenocarcinomas,” Histopathology 56, 921–931 (2010).
[Crossref]

Barr, H.

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

Beleites, C.

C. Beleites, C. Krafft, J. Popp, and V. Sergo, “HyperSpec: working with spectroscopic data,” in R User Conference, useR!, August16, 2011.

Bhargava, R.

S. Mittal, K. Yeh, L. S. Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

S. Mittal, K. L. S. Yeh Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

R. Bhargava, “Infrared spectroscopic imaging: the next generation,” Appl. Spectrosc. 66, 1091–1120 (2012).
[Crossref]

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol. 23, 469–474 (2005).
[Crossref]

Brandstrup Morrish, R.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

Brown, M. D.

M. J. Pilling, A. Henderson, J. H. Shanks, M. D. Brown, N. W. Clarke, and P. Gardner, “Infrared spectral histopathology using haematoxylin and eosin (H&E) stained glass slides: a major step forward towards clinical translation,” Analyst 142, 1258–1268 (2017).
[Crossref]

Carranza, E. J. M.

D. F. Meer, H. M. A. Werff, F. J. A. Ruitenbeek, C. A. Hecker, W. H. Bakker, M. F. Noomen, M. Meijde, E. J. M. Carranza, J. B. Smeth, and T. Woldai, “Multi and hyperspectral geologic remote sensing: A review,” Int. J. Appl. Earth Obs. Geinf. 14, 112–128 (2012).
[Crossref]

Chaitanya Kumar, S.

M. Ebrahim-Zadeh and S. Chaitanya Kumar, “Yb-fiber-laser-pumped ultrafast frequency conversion sources from the mid-Infrared to the ultraviolet,” IEEE J. Sel. Top. Quantum Electron. 20, 7600519 (2014).
[Crossref]

Chan, C. H.

Clarke, N. W.

M. J. Pilling, A. Henderson, J. H. Shanks, M. D. Brown, N. W. Clarke, and P. Gardner, “Infrared spectral histopathology using haematoxylin and eosin (H&E) stained glass slides: a major step forward towards clinical translation,” Analyst 142, 1258–1268 (2017).
[Crossref]

Dam, J. S.

Demur, R.

Drummond, L.

Ebrahim-Zadeh, M.

M. Ebrahim-Zadeh and S. Chaitanya Kumar, “Yb-fiber-laser-pumped ultrafast frequency conversion sources from the mid-Infrared to the ultraviolet,” IEEE J. Sel. Top. Quantum Electron. 20, 7600519 (2014).
[Crossref]

Fabre, C.

Fernandez, D. C.

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol. 23, 469–474 (2005).
[Crossref]

Fischer, H.

Forgue-Lafitte, M. E.

A. Travo, O. Piot, R. Wolthuis, C. Gobinet, M. Manfait, J. Bara, M. E. Forgue-Lafitte, and P. Jeanneson, “IR spectral imaging of secreted mucus: a promising new tool for the histopathological recognition of human colonic adenocarcinomas,” Histopathology 56, 921–931 (2010).
[Crossref]

Gardner, P.

M. J. Pilling, A. Henderson, J. H. Shanks, M. D. Brown, N. W. Clarke, and P. Gardner, “Infrared spectral histopathology using haematoxylin and eosin (H&E) stained glass slides: a major step forward towards clinical translation,” Analyst 142, 1258–1268 (2017).
[Crossref]

Geladi, P.

H. F. Grahn and P. Geladi, Techniques and Applications of Hyperspectral Image Analysis (Wiley, 2007).

Gerwert, K.

C. Kuepper, A. Kallenbach-Thieltges, H. Juette, A. Tannapfel, F. Großerueschkamp, and K. Gerwert, “Quantum cascade laser based infrared microscopy for label-free and automated cancer classification in tissue sections,” Sci. Rep. 8, 7717 (2018).
[Crossref]

Gobinet, C.

A. Travo, O. Piot, R. Wolthuis, C. Gobinet, M. Manfait, J. Bara, M. E. Forgue-Lafitte, and P. Jeanneson, “IR spectral imaging of secreted mucus: a promising new tool for the histopathological recognition of human colonic adenocarcinomas,” Histopathology 56, 921–931 (2010).
[Crossref]

Goodman, J. W.

J. W. Goodman, “Optical methods for suppressing speckle,” in Speckle Phenomena in Optics (Roberts & Company, 2007), pp. 141–186.

Grahn, H. F.

H. F. Grahn and P. Geladi, Techniques and Applications of Hyperspectral Image Analysis (Wiley, 2007).

Graioud, R.

Grisard, A.

Großerueschkamp, F.

C. Kuepper, A. Kallenbach-Thieltges, H. Juette, A. Tannapfel, F. Großerueschkamp, and K. Gerwert, “Quantum cascade laser based infrared microscopy for label-free and automated cancer classification in tissue sections,” Sci. Rep. 8, 7717 (2018).
[Crossref]

Hanna, D. C.

M. J. T. Milton, T. J. McIlveen, D. C. Hanna, and P. T. Woods, “High-efficiency infrared generation by difference-frequency mixing using tangential phase matching,” Opt. Commun. 87, 273–277 (1992).
[Crossref]

Hartigan, J. A.

J. A. Hartigan and M. A. Wong, “A K-means clustering algorithm,” Appl. Statist. 28, 100–108 (1979).
[Crossref]

He, T.

W. Wang, S. Liang, T. He, and O. Shi, “Estimating clear-sky all-wave net radiation from combined visible and shortwave infrared (VSWIR) and thermal infrared (TIR) remote sensing data,” Remote Sens. Environ. 167, 31–39 (2015).
[Crossref]

Hecker, C. A.

D. F. Meer, H. M. A. Werff, F. J. A. Ruitenbeek, C. A. Hecker, W. H. Bakker, M. F. Noomen, M. Meijde, E. J. M. Carranza, J. B. Smeth, and T. Woldai, “Multi and hyperspectral geologic remote sensing: A review,” Int. J. Appl. Earth Obs. Geinf. 14, 112–128 (2012).
[Crossref]

Henderson, A.

M. J. Pilling, A. Henderson, J. H. Shanks, M. D. Brown, N. W. Clarke, and P. Gardner, “Infrared spectral histopathology using haematoxylin and eosin (H&E) stained glass slides: a major step forward towards clinical translation,” Analyst 142, 1258–1268 (2017).
[Crossref]

Hermes, M.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

J. Nallala, G. R. Lloyd, M. Hermes, N. Shepherd, and N. Stone, “Enhanced spectral histology in the colon using high-magnification benchtop FTIR imaging,” Vib. Spectrosc. 91, 83–91 (2016).
[Crossref]

Hewitt, S. M.

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol. 23, 469–474 (2005).
[Crossref]

Høgstedt, L.

Houghton, J.

J. Houghton, “Global warming,” Rep. Prog. Phys. 68, 1343–1403(2005).
[Crossref]

Huot, L.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

Isabelle, M.

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

Jeanneson, P.

A. Travo, O. Piot, R. Wolthuis, C. Gobinet, M. Manfait, J. Bara, M. E. Forgue-Lafitte, and P. Jeanneson, “IR spectral imaging of secreted mucus: a promising new tool for the histopathological recognition of human colonic adenocarcinomas,” Histopathology 56, 921–931 (2010).
[Crossref]

Juette, H.

C. Kuepper, A. Kallenbach-Thieltges, H. Juette, A. Tannapfel, F. Großerueschkamp, and K. Gerwert, “Quantum cascade laser based infrared microscopy for label-free and automated cancer classification in tissue sections,” Sci. Rep. 8, 7717 (2018).
[Crossref]

Junaid, S.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

S. Junaid, J. Tomko, W. T. Masselink, C. Pedersen, and P. Tidemand-Lichtenberg, “Mid-infrared upconversion based hyperspectral imaging,” Opt. Express 26, 2203–2211 (2018).
[Crossref]

Kajdacsy-Balla, A.

S. Mittal, K. L. S. Yeh Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

S. Mittal, K. Yeh, L. S. Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

Kallenbach-Thieltges, A.

C. Kuepper, A. Kallenbach-Thieltges, H. Juette, A. Tannapfel, F. Großerueschkamp, and K. Gerwert, “Quantum cascade laser based infrared microscopy for label-free and automated cancer classification in tissue sections,” Sci. Rep. 8, 7717 (2018).
[Crossref]

Kastl, L.

F. Penaranda, V. Naranjo, L. Kastl, B. Kemper, G. R. Lloyd, J. Nallala, N. Stone, and J. Schnekenberger, “Multivariate classification of Fourier transform infrared hyperspectral images of skin cancer cells,” in IEEE European Signal Processing Conference (2016), pp. 1328–1332.

Kehlet, L. M.

Kemper, B.

F. Penaranda, V. Naranjo, L. Kastl, B. Kemper, G. R. Lloyd, J. Nallala, N. Stone, and J. Schnekenberger, “Multivariate classification of Fourier transform infrared hyperspectral images of skin cancer cells,” in IEEE European Signal Processing Conference (2016), pp. 1328–1332.

Kendall, C.

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

Kenkel, S.

S. Mittal, K. Yeh, L. S. Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

S. Mittal, K. L. S. Yeh Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

Königstedt, R.

Krafft, C.

C. Beleites, C. Krafft, J. Popp, and V. Sergo, “HyperSpec: working with spectroscopic data,” in R User Conference, useR!, August16, 2011.

Kuepper, C.

C. Kuepper, A. Kallenbach-Thieltges, H. Juette, A. Tannapfel, F. Großerueschkamp, and K. Gerwert, “Quantum cascade laser based infrared microscopy for label-free and automated cancer classification in tissue sections,” Sci. Rep. 8, 7717 (2018).
[Crossref]

Lallier, E.

Leslie, L. S.

S. Mittal, K. Yeh, L. S. Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

Leviandier, L.

Levin, I. W.

D. C. Fernandez, R. Bhargava, S. M. Hewitt, and I. W. Levin, “Infrared spectroscopic imaging for histopathologic recognition,” Nat. Biotechnol. 23, 469–474 (2005).
[Crossref]

Li, J.

Li, Z.

Liang, S.

W. Wang, S. Liang, T. He, and O. Shi, “Estimating clear-sky all-wave net radiation from combined visible and shortwave infrared (VSWIR) and thermal infrared (TIR) remote sensing data,” Remote Sens. Environ. 167, 31–39 (2015).
[Crossref]

Lloyd, G. R.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

J. Nallala, G. R. Lloyd, M. Hermes, N. Shepherd, and N. Stone, “Enhanced spectral histology in the colon using high-magnification benchtop FTIR imaging,” Vib. Spectrosc. 91, 83–91 (2016).
[Crossref]

G. R. Lloyd and N. Stone, “Method for identification of spectral targets in discrete frequency infrared spectroscopy for clinical diagnostics,” Appl. Spectrosc. 69, 1066–1073 (2015).
[Crossref]

F. Penaranda, V. Naranjo, L. Kastl, B. Kemper, G. R. Lloyd, J. Nallala, N. Stone, and J. Schnekenberger, “Multivariate classification of Fourier transform infrared hyperspectral images of skin cancer cells,” in IEEE European Signal Processing Conference (2016), pp. 1328–1332.

Manfait, M.

A. Travo, O. Piot, R. Wolthuis, C. Gobinet, M. Manfait, J. Bara, M. E. Forgue-Lafitte, and P. Jeanneson, “IR spectral imaging of secreted mucus: a promising new tool for the histopathological recognition of human colonic adenocarcinomas,” Histopathology 56, 921–931 (2010).
[Crossref]

Masselink, W. T.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

S. Junaid, J. Tomko, W. T. Masselink, C. Pedersen, and P. Tidemand-Lichtenberg, “Mid-infrared upconversion based hyperspectral imaging,” Opt. Express 26, 2203–2211 (2018).
[Crossref]

Mathez, M.

McIlveen, T. J.

M. J. T. Milton, T. J. McIlveen, D. C. Hanna, and P. T. Woods, “High-efficiency infrared generation by difference-frequency mixing using tangential phase matching,” Opt. Commun. 87, 273–277 (1992).
[Crossref]

Meer, D. F.

D. F. Meer, H. M. A. Werff, F. J. A. Ruitenbeek, C. A. Hecker, W. H. Bakker, M. F. Noomen, M. Meijde, E. J. M. Carranza, J. B. Smeth, and T. Woldai, “Multi and hyperspectral geologic remote sensing: A review,” Int. J. Appl. Earth Obs. Geinf. 14, 112–128 (2012).
[Crossref]

Meijde, M.

D. F. Meer, H. M. A. Werff, F. J. A. Ruitenbeek, C. A. Hecker, W. H. Bakker, M. F. Noomen, M. Meijde, E. J. M. Carranza, J. B. Smeth, and T. Woldai, “Multi and hyperspectral geologic remote sensing: A review,” Int. J. Appl. Earth Obs. Geinf. 14, 112–128 (2012).
[Crossref]

Meng, L.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

Milton, M. J. T.

M. J. T. Milton, T. J. McIlveen, D. C. Hanna, and P. T. Woods, “High-efficiency infrared generation by difference-frequency mixing using tangential phase matching,” Opt. Commun. 87, 273–277 (1992).
[Crossref]

Mittal, S.

S. Mittal, K. Yeh, L. S. Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

S. Mittal, K. L. S. Yeh Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

Mlynczak, M. G.

M. N. Abedin, M. G. Mlynczak, and T. F. Refaat, “Infrared detectors overview in the short-wave infrared to far-infrared for CLARREO mission,” Proc. SPIE 7808, 780801 (2010).
[Crossref]

Morvan, L.

Nallala, J.

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

J. Nallala, G. R. Lloyd, M. Hermes, N. Shepherd, and N. Stone, “Enhanced spectral histology in the colon using high-magnification benchtop FTIR imaging,” Vib. Spectrosc. 91, 83–91 (2016).
[Crossref]

F. Penaranda, V. Naranjo, L. Kastl, B. Kemper, G. R. Lloyd, J. Nallala, N. Stone, and J. Schnekenberger, “Multivariate classification of Fourier transform infrared hyperspectral images of skin cancer cells,” in IEEE European Signal Processing Conference (2016), pp. 1328–1332.

Naranjo, V.

F. Penaranda, V. Naranjo, L. Kastl, B. Kemper, G. R. Lloyd, J. Nallala, N. Stone, and J. Schnekenberger, “Multivariate classification of Fourier transform infrared hyperspectral images of skin cancer cells,” in IEEE European Signal Processing Conference (2016), pp. 1328–1332.

Noomen, M. F.

D. F. Meer, H. M. A. Werff, F. J. A. Ruitenbeek, C. A. Hecker, W. H. Bakker, M. F. Noomen, M. Meijde, E. J. M. Carranza, J. B. Smeth, and T. Woldai, “Multi and hyperspectral geologic remote sensing: A review,” Int. J. Appl. Earth Obs. Geinf. 14, 112–128 (2012).
[Crossref]

Old, O. J.

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

Otto, W. R.

Palombo, F.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

Parchatka, U.

Pedersen, C.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

S. Junaid, J. Tomko, W. T. Masselink, C. Pedersen, and P. Tidemand-Lichtenberg, “Mid-infrared upconversion based hyperspectral imaging,” Opt. Express 26, 2203–2211 (2018).
[Crossref]

M. Mathez, P. J. Rodrigo, P. Tidemand-Lichtenberg, and C. Pedersen, “Upconversion imaging using short-wave infrared picosecond pulses,” Opt. Lett. 42, 579–582 (2017).
[Crossref]

L. M. Kehlet, N. Sanders, P. Tidemand-Lichtenberg, J. S. Dam, and C. Pedersen, “Infrared hyperspectral upconversion imaging using spatial object translation,” Opt. Express 23, 34023–34027 (2015).
[Crossref]

L. M. Kehlet, P. Tidemand-Lichtenberg, J. S. Dam, and C. Pedersen, “Infrared upconversion hyperspectral imaging,” Opt. Lett. 40, 938–941 (2015).
[Crossref]

L. Høgstedt, J. S. Dam, A.-L. Sahlberg, Z. Li, M. Aldén, C. Pedersen, and P. Tidemand-Lichtenberg, “Low-noise mid-IR upconversion detector for improved IR-degenerate four-wave mixing gas sensing,” Opt. Lett. 39, 5321–5324 (2014).
[Crossref]

J. S. Dam, C. Pedersen, and P. Tidemand-Lichtenberg, “Theory for upconversion of incoherent images,” Opt. Express 20, 1475–1482 (2012).
[Crossref]

J. S. Dam, P. Tidemand-Lichtenberg, and C. Pedersen, “Room-temperature mid-infrared single-photon spectral imaging,” Nat. Photonics 6, 788–793 (2012).
[Crossref]

Penaranda, F.

F. Penaranda, V. Naranjo, L. Kastl, B. Kemper, G. R. Lloyd, J. Nallala, N. Stone, and J. Schnekenberger, “Multivariate classification of Fourier transform infrared hyperspectral images of skin cancer cells,” in IEEE European Signal Processing Conference (2016), pp. 1328–1332.

Phillips, C.

Pilling, M. J.

M. J. Pilling, A. Henderson, J. H. Shanks, M. D. Brown, N. W. Clarke, and P. Gardner, “Infrared spectral histopathology using haematoxylin and eosin (H&E) stained glass slides: a major step forward towards clinical translation,” Analyst 142, 1258–1268 (2017).
[Crossref]

Piot, O.

A. Travo, O. Piot, R. Wolthuis, C. Gobinet, M. Manfait, J. Bara, M. E. Forgue-Lafitte, and P. Jeanneson, “IR spectral imaging of secreted mucus: a promising new tool for the histopathological recognition of human colonic adenocarcinomas,” Histopathology 56, 921–931 (2010).
[Crossref]

Popp, J.

C. Beleites, C. Krafft, J. Popp, and V. Sergo, “HyperSpec: working with spectroscopic data,” in R User Conference, useR!, August16, 2011.

Refaat, T. F.

M. N. Abedin, M. G. Mlynczak, and T. F. Refaat, “Infrared detectors overview in the short-wave infrared to far-infrared for CLARREO mission,” Proc. SPIE 7808, 780801 (2010).
[Crossref]

Rodrigo, P. J.

Rogalski, A.

A. Rogalski, “Infrared detectors: an overview,” Infrared Phys. Technol. 43, 187–210 (2002).
[Crossref]

Ruitenbeek, F. J. A.

D. F. Meer, H. M. A. Werff, F. J. A. Ruitenbeek, C. A. Hecker, W. H. Bakker, M. F. Noomen, M. Meijde, E. J. M. Carranza, J. B. Smeth, and T. Woldai, “Multi and hyperspectral geologic remote sensing: A review,” Int. J. Appl. Earth Obs. Geinf. 14, 112–128 (2012).
[Crossref]

Sahlberg, A.-L.

Sanders, N.

Schnekenberger, J.

F. Penaranda, V. Naranjo, L. Kastl, B. Kemper, G. R. Lloyd, J. Nallala, N. Stone, and J. Schnekenberger, “Multivariate classification of Fourier transform infrared hyperspectral images of skin cancer cells,” in IEEE European Signal Processing Conference (2016), pp. 1328–1332.

Sergo, V.

C. Beleites, C. Krafft, J. Popp, and V. Sergo, “HyperSpec: working with spectroscopic data,” in R User Conference, useR!, August16, 2011.

Shanks, J. H.

M. J. Pilling, A. Henderson, J. H. Shanks, M. D. Brown, N. W. Clarke, and P. Gardner, “Infrared spectral histopathology using haematoxylin and eosin (H&E) stained glass slides: a major step forward towards clinical translation,” Analyst 142, 1258–1268 (2017).
[Crossref]

Shepherd, N.

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

J. Nallala, G. R. Lloyd, M. Hermes, N. Shepherd, and N. Stone, “Enhanced spectral histology in the colon using high-magnification benchtop FTIR imaging,” Vib. Spectrosc. 91, 83–91 (2016).
[Crossref]

Shi, O.

W. Wang, S. Liang, T. He, and O. Shi, “Estimating clear-sky all-wave net radiation from combined visible and shortwave infrared (VSWIR) and thermal infrared (TIR) remote sensing data,” Remote Sens. Environ. 167, 31–39 (2015).
[Crossref]

Shore, A. C.

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

Smeth, J. B.

D. F. Meer, H. M. A. Werff, F. J. A. Ruitenbeek, C. A. Hecker, W. H. Bakker, M. F. Noomen, M. Meijde, E. J. M. Carranza, J. B. Smeth, and T. Woldai, “Multi and hyperspectral geologic remote sensing: A review,” Int. J. Appl. Earth Obs. Geinf. 14, 112–128 (2012).
[Crossref]

Stone, N.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

J. Nallala, G. R. Lloyd, M. Hermes, N. Shepherd, and N. Stone, “Enhanced spectral histology in the colon using high-magnification benchtop FTIR imaging,” Vib. Spectrosc. 91, 83–91 (2016).
[Crossref]

G. R. Lloyd and N. Stone, “Method for identification of spectral targets in discrete frequency infrared spectroscopy for clinical diagnostics,” Appl. Spectrosc. 69, 1066–1073 (2015).
[Crossref]

F. Penaranda, V. Naranjo, L. Kastl, B. Kemper, G. R. Lloyd, J. Nallala, N. Stone, and J. Schnekenberger, “Multivariate classification of Fourier transform infrared hyperspectral images of skin cancer cells,” in IEEE European Signal Processing Conference (2016), pp. 1328–1332.

Sun, D.-W.

D.-W. Sun, Hyperspectral Imaging for Food Quality Analysis and Control (Academic, 2010).

Tannapfel, A.

C. Kuepper, A. Kallenbach-Thieltges, H. Juette, A. Tannapfel, F. Großerueschkamp, and K. Gerwert, “Quantum cascade laser based infrared microscopy for label-free and automated cancer classification in tissue sections,” Sci. Rep. 8, 7717 (2018).
[Crossref]

Tidemand-Lichtenberg, P.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

S. Junaid, J. Tomko, W. T. Masselink, C. Pedersen, and P. Tidemand-Lichtenberg, “Mid-infrared upconversion based hyperspectral imaging,” Opt. Express 26, 2203–2211 (2018).
[Crossref]

M. Mathez, P. J. Rodrigo, P. Tidemand-Lichtenberg, and C. Pedersen, “Upconversion imaging using short-wave infrared picosecond pulses,” Opt. Lett. 42, 579–582 (2017).
[Crossref]

L. M. Kehlet, N. Sanders, P. Tidemand-Lichtenberg, J. S. Dam, and C. Pedersen, “Infrared hyperspectral upconversion imaging using spatial object translation,” Opt. Express 23, 34023–34027 (2015).
[Crossref]

L. M. Kehlet, P. Tidemand-Lichtenberg, J. S. Dam, and C. Pedersen, “Infrared upconversion hyperspectral imaging,” Opt. Lett. 40, 938–941 (2015).
[Crossref]

L. Høgstedt, J. S. Dam, A.-L. Sahlberg, Z. Li, M. Aldén, C. Pedersen, and P. Tidemand-Lichtenberg, “Low-noise mid-IR upconversion detector for improved IR-degenerate four-wave mixing gas sensing,” Opt. Lett. 39, 5321–5324 (2014).
[Crossref]

J. S. Dam, C. Pedersen, and P. Tidemand-Lichtenberg, “Theory for upconversion of incoherent images,” Opt. Express 20, 1475–1482 (2012).
[Crossref]

J. S. Dam, P. Tidemand-Lichtenberg, and C. Pedersen, “Room-temperature mid-infrared single-photon spectral imaging,” Nat. Photonics 6, 788–793 (2012).
[Crossref]

Tomko, J.

M. Hermes, R. Brandstrup Morrish, L. Huot, L. Meng, S. Junaid, J. Tomko, G. R. Lloyd, W. T. Masselink, P. Tidemand-Lichtenberg, C. Pedersen, F. Palombo, and N. Stone, “Mid-IR hyperspectral imaging for label-free histopathology and cytology,” J. Opt. 20, 023002 (2018).
[Crossref]

S. Junaid, J. Tomko, W. T. Masselink, C. Pedersen, and P. Tidemand-Lichtenberg, “Mid-infrared upconversion based hyperspectral imaging,” Opt. Express 26, 2203–2211 (2018).
[Crossref]

Travo, A.

A. Travo, O. Piot, R. Wolthuis, C. Gobinet, M. Manfait, J. Bara, M. E. Forgue-Lafitte, and P. Jeanneson, “IR spectral imaging of secreted mucus: a promising new tool for the histopathological recognition of human colonic adenocarcinomas,” Histopathology 56, 921–931 (2010).
[Crossref]

Treps, N.

Wang, W.

W. Wang, S. Liang, T. He, and O. Shi, “Estimating clear-sky all-wave net radiation from combined visible and shortwave infrared (VSWIR) and thermal infrared (TIR) remote sensing data,” Remote Sens. Environ. 167, 31–39 (2015).
[Crossref]

Warner, J.

J. Warner, “Phase-matching for optical up-conversion with maximum angular aperture—theory and practice,” Opto-Electronics 1, 25–28 (1969).
[Crossref]

Werff, H. M. A.

D. F. Meer, H. M. A. Werff, F. J. A. Ruitenbeek, C. A. Hecker, W. H. Bakker, M. F. Noomen, M. Meijde, E. J. M. Carranza, J. B. Smeth, and T. Woldai, “Multi and hyperspectral geologic remote sensing: A review,” Int. J. Appl. Earth Obs. Geinf. 14, 112–128 (2012).
[Crossref]

Woldai, T.

D. F. Meer, H. M. A. Werff, F. J. A. Ruitenbeek, C. A. Hecker, W. H. Bakker, M. F. Noomen, M. Meijde, E. J. M. Carranza, J. B. Smeth, and T. Woldai, “Multi and hyperspectral geologic remote sensing: A review,” Int. J. Appl. Earth Obs. Geinf. 14, 112–128 (2012).
[Crossref]

Wolthuis, R.

A. Travo, O. Piot, R. Wolthuis, C. Gobinet, M. Manfait, J. Bara, M. E. Forgue-Lafitte, and P. Jeanneson, “IR spectral imaging of secreted mucus: a promising new tool for the histopathological recognition of human colonic adenocarcinomas,” Histopathology 56, 921–931 (2010).
[Crossref]

Wong, M. A.

J. A. Hartigan and M. A. Wong, “A K-means clustering algorithm,” Appl. Statist. 28, 100–108 (1979).
[Crossref]

Woods, P. T.

M. J. T. Milton, T. J. McIlveen, D. C. Hanna, and P. T. Woods, “High-efficiency infrared generation by difference-frequency mixing using tangential phase matching,” Opt. Commun. 87, 273–277 (1992).
[Crossref]

Wright, N. A.

Yeh, K.

S. Mittal, K. Yeh, L. S. Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

Yeh Leslie, K. L. S.

S. Mittal, K. L. S. Yeh Leslie, S. Kenkel, A. Kajdacsy-Balla, and R. Bhargava, “Simultaneous cancer and tumor microenvironment subtyping using confocal infrared microscopy for all-digital molecular histopathology,” Proc. Natl. Acad. Sci. USA 115, E5651–E5660 (2018).
[Crossref]

Analyst (2)

O. J. Old, G. R. Lloyd, J. Nallala, M. Isabelle, M. Almond, C. Kendall, N. Shepherd, A. C. Shore, H. Barr, and N. Stone, “Rapid infrared mapping for highly accurate automated histology in Barrett’s oesophagus,” Analyst 142, 1227–1234 (2017).
[Crossref]

M. J. Pilling, A. Henderson, J. H. Shanks, M. D. Brown, N. W. Clarke, and P. Gardner, “Infrared spectral histopathology using haematoxylin and eosin (H&E) stained glass slides: a major step forward towards clinical translation,” Analyst 142, 1258–1268 (2017).
[Crossref]

Appl. Spectrosc. (2)

Appl. Statist. (1)

J. A. Hartigan and M. A. Wong, “A K-means clustering algorithm,” Appl. Statist. 28, 100–108 (1979).
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Histopathology (1)

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Supplementary Material (4)

NameDescription
» Supplement 1       supplemental document
» Visualization 1       Increased FoV upconverted monochromatic images using angular tuning of the nonlinear crystal, with resolution target.
» Visualization 2       Increased FoV upconverted monochromatic images using angular tuning of the nonlinear crystal, without resolution target.
» Visualization 3       High speed post-processing free monochromatic imaging, with butane sprayed from a gas lighter in the object plane with relosution target. Measured at the absorption line of butane at 3.37 µm.

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Figures (6)

Fig. 1.
Fig. 1. Setup for the upconversion-based imaging, where the idler beam from a picosecond OPO is used as an illumination source and a synchronized picosecond 1064 nm laser source is used as the pump source. The beams are spatially and temporally overlapped in the nonlinear crystal (lithium niobate) for efficient upconversion. The phase-match condition is scanned by rotating the crystal in synchronism with the camera integration time. Lenses, f1 (50 mm) and f2 (50 mm, 100 mm), are used at the front and back focal plane of the 4f setup. Filters (shortpass 950 nm, longpass 700 nm) blocks residual unwanted stray light.
Fig. 2.
Fig. 2. Model of the upconversion process comprising three steps. The original mid-IR object is first rescaled, then convolved with the point spread function, which, in our case, is a Gaussian pump beam. Finally, the phase-match condition is multiplied to form the upconverted image. Multiplication of the sinc2 term rather than convolution (i.e., blurring) is vital for superimposing different ring patterns to form a single upconverted image with increase FoV.
Fig. 3.
Fig. 3. (a)–(c) Upconverted images of a USAF resolution target at 3.1 μm by varying the crystal rotation angle (4.7°, 4.3°, 4.0°), (d)–(f) the corresponding simulated images at the same angles validating the proposed model shown in Fig. 2.
Fig. 4.
Fig. 4. (a) Upconverted image of the resolution target at 3.1 μm when rotating the crystal from 4.7° to 3.7° with respect to c axis and in synchronism with the camera. The camera integration time per frame is 2.5 ms. (b) A magnified version of the smallest features of the resolution target corresponding to the square box in (a), f2 was changed from 50 to 100 mm focal length to increase magnification. (c) Intensity profile along the white line in (b); the pink circle highlights the smallest features.
Fig. 5.
Fig. 5. (a) Setup for the imaging of the tissue sample. The original size of the beam emitted from the OPO is 10 mm, which is reduced to 2 mm, using a pair of lenses: f3 and f6=250mm, f4 and f5=50mm. (b) Image of the tissue sample acquired using upconversion at 3.34 μm wavelength. (c) Image when using incoherent illumination (approx. 10,000 intensity levels).
Fig. 6.
Fig. 6. (Top row) Images of the tissue sample acquired using FTIR and upconversion, Spectral analysis of the cancerous and healthy tissue sample, based on upconversion imaging and FTIR. (Bottom row) Stained biopsies evaluated by a pathologist and color-coded according to pathologies annotated.