Abstract

In brain tumor surgery, recognition of tumor boundaries is key. However, intraoperative assessment of tumor boundaries by the neurosurgeon is difficult. Therefore, there is an urgent need for tools that provide the neurosurgeon with pathological information during the operation. We show that third harmonic generation (THG) microscopy provides label-free, real-time images of histopathological quality; increased cellularity, nuclear pleomorphism, and rarefaction of neuropil in fresh, unstained human brain tissue could be clearly recognized. We further demonstrate THG images taken with a GRIN objective, as a step toward in situ THG microendoscopy of tumor boundaries. THG imaging is thus a promising tool for optical biopsies.

© 2016 Optical Society of America

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2015 (7)

T. Hollon, S. L. Hervey-Jumper, O. Sagher, and D. A. Orringer, “Advances in the Surgical Management of Low-Grade Glioma,” Semin. Radiat. Oncol. 25(3), 181–188 (2015).
[Crossref] [PubMed]

O. van Tellingen, B. Yetkin-Arik, M. C. de Gooijer, P. Wesseling, T. Wurdinger, and H. E. de Vries, “Overcoming the blood-brain tumor barrier for effective glioblastoma treatment,” Drug Resist. Updat. 19, 1–12 (2015).
[Crossref] [PubMed]

C. Kut, K. L. Chaichana, J. Xi, S. M. Raza, X. Ye, E. R. McVeigh, F. J. Rodriguez, A. Quiñones-Hinojosa, and X. Li, “Detection of human brain cancer infiltration ex vivo and in vivo using quantitative optical coherence tomography,” Sci. Transl. Med. 7(292), ra100 (2015).
[Crossref] [PubMed]

M. Ji, S. Lewis, S. Camelo-Piragua, S. H. Ramkissoon, M. Snuderl, S. Venneti, A. Fisher-Hubbard, M. Garrard, D. Fu, A. C. Wang, J. A. Heth, C. O. Maher, N. Sanai, T. D. Johnson, C. W. Freudiger, O. Sagher, X. S. Xie, and D. A. Orringer, “Detection of human brain tumor infiltration with quantitative stimulated Raman scattering microscopy,” Sci. Transl. Med. 7(309), 309ra163 (2015).
[Crossref] [PubMed]

M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette, K. Saint-Arnaud, L. Bernstein, M. C. Guiot, K. Petrecca, and F. Leblond, “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Med. 7(274), ra19 (2015).
[Crossref] [PubMed]

P. C. Wu, T. Y. Hsieh, Z. U. Tsai, and T. M. Liu, “In vivo quantification of the structural changes of collagens in a melanoma microenvironment with second and third harmonic generation microscopy,” Sci. Rep. 5, 8879 (2015).
[Crossref] [PubMed]

J. Duran and J. J. Guinovart, “Brain glycogen in health and disease,” Mol. Aspects Med. 46, 70–77 (2015).
[Crossref] [PubMed]

2014 (7)

A. Khanna, K. T. Kahle, B. P. Walcott, V. Gerzanich, and J. M. Simard, “Disruption of Ion Homeostasis in the Neurogliovascular Unit Underlies the Pathogenesis of Ischemic Cerebral Edema,” Transl. Stroke Res. 5(1), 3–16 (2014).
[Crossref] [PubMed]

D. M. Huland, M. Jain, D. G. Ouzounov, B. D. Robinson, D. S. Harya, M. M. Shevchuk, P. Singhal, C. Xu, and A. K. Tewari, “Multiphoton gradient index endoscopy for evaluation of diseased human prostatic tissue ex vivo,” J. Biomed. Opt. 19(11), 116011 (2014).
[Crossref] [PubMed]

G. Thomas, O. Nadiarnykh, J. van Voskuilen, C. L. Hoy, H. C. Gerritsen, and H. J. Sterenborg, “Estimating the risk of squamous cell cancer induction in skin following nonlinear optical imaging,” J. Biophotonics 7(7), 492–505 (2014).
[Crossref] [PubMed]

H. Lim, D. Sharoukhov, I. Kassim, Y. Zhang, J. L. Salzer, and C. V. Melendez-Vasquez, “Label-free imaging of Schwann cell myelination by third harmonic generation microscopy,” Proc. Natl. Acad. Sci. USA 111(50), 18025–18030 (2014).

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, “Label-free imaging of lipid depositions in C. elegans using third-harmonic generation microscopy,” PLoS One 9(1), e84431 (2014).
[Crossref] [PubMed]

W. Stummer, J. C. Tonn, C. Goetz, W. Ullrich, H. Stepp, A. Bink, T. Pietsch, and U. Pichlmeier, “5-Aminolevulinic Acid-Derived Tumor Fluorescence: The Diagnostic Accuracy of Visible Fluorescence Qualities as Corroborated by Spectrometry and Histology and Postoperative Imaging,” Neurosurgery 74(3), 310–320 (2014).
[Crossref] [PubMed]

Y. Li, R. Rey-Dios, D. W. Roberts, P. A. Valdés, and A. A. Cohen-Gadol, “Intraoperative Fluorescence-Guided Resection of High-Grade Gliomas: A Comparison of the Present Techniques and Evolution of Future Strategies,” World. Neurosurg. 82(1-2), 175–185 (2014).
[Crossref] [PubMed]

2013 (5)

I. Y. Eyüpoglu, M. Buchfelder, and N. E. Savaskan, “Surgical resection of malignant gliomas-role in optimizing patient outcome,” Nat. Rev. Neurol. 9(3), 141–151 (2013).
[Crossref] [PubMed]

M. Ji, D. A. Orringer, C. W. Freudiger, S. Ramkissoon, X. Liu, D. Lau, A. J. Golby, I. Norton, M. Hayashi, N. Y. Agar, G. S. Young, C. Spino, S. Santagata, S. Camelo-Piragua, K. L. Ligon, O. Sagher, and X. S. Xie, “Rapid, label-free detection of brain tumors with stimulated Raman scattering microscopy,” Sci. Transl. Med. 5(201), 201ra119 (2013).
[Crossref] [PubMed]

Z. X. Lin, “Glioma-related edema: new insight into molecular mechanisms and their clinical implications,” Chin. J. Cancer 32(1), 49–52 (2013).
[Crossref] [PubMed]

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[Crossref] [PubMed]

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[Crossref] [PubMed]

2012 (5)

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]

C. M. Brown, D. R. Rivera, I. Pavlova, D. G. Ouzounov, W. O. Williams, S. Mohanan, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using a compact and flexible multiphoton microendoscope,” J. Biomed. Opt. 17(4), 040505 (2012).
[Crossref] [PubMed]

T. A. Murray and M. J. Levene, “Singlet gradient index lens for deep in vivo multiphoton microscopy,” J. Biomed. Opt. 17(2), 021106 (2012).
[Crossref] [PubMed]

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, D. B. Almeida, L. A. Andrade, F. Bottcher-Luiz, H. F. Carvalho, and C. L. Cesar, “Optical biomarkers of serous and mucinous human ovarian tumor assessed with nonlinear optics microscopies,” PLoS One 7(10), e47007 (2012).
[Crossref] [PubMed]

B. Weigelin, G.-J. Bakker, and P. Friedl, “Intravital third harmonic generation microscopy of collective melanoma cell invasion,” Intra.Vital 1(1), 32–43 (2012).

2011 (5)

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. Louise Groot, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 108(15), 5970–5975 (2011).
[Crossref] [PubMed]

P. Mahou, N. Olivier, G. Labroille, L. Duloquin, J. M. Sintes, N. Peyriéras, R. Legouis, D. Débarre, and E. Beaurepaire, “Combined third-harmonic generation and four-wave mixing microscopy of tissues and embryos,” Biomed. Opt. Express 2(10), 2837–2849 (2011).
[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]

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]

J. P. Zinter and M. J. Levene, “Maximizing fluorescence collection efficiency in multiphoton microscopy,” Opt. Express 19(16), 15348–15362 (2011).
[Crossref] [PubMed]

2010 (5)

S.-H. Chia, C.-H. Yu, C.-H. Lin, N.-C. Cheng, T.-M. Liu, M.-C. Chan, I. H. Chen, and C.-K. Sun, “Miniaturized video-rate epi-third-harmonic-generation fiber-microscope,” Opt. Express 18(16), 17382–17391 (2010).
[Crossref] [PubMed]

J. M. Dela Cruz, J. D. McMullen, R. M. Williams, and W. R. Zipfel, “Feasibility of using multiphoton excited tissue autofluorescence for in vivo human histopathology,” Biomed. Opt. Express 1(5), 1320–1330 (2010).
[Crossref] [PubMed]

M. Hefti, H. M. Mehdorn, I. Albert, and L. Dorner, “Fluorescence-Guided Surgery for Malignant Glioma: A Review on Aminolevulinic Acid Induced Protoporphyrin IX Photodynamic Diagnostic in Brain Tumors,” Curr. Med. Imaging Rev. 6(4), 254–258 (2010).
[Crossref]

G. Testa-Silva, M. B. Verhoog, N. A. Goriounova, A. Loebel, J. Hjorth, J. C. Baayen, C. P. J. de Kock, and H. D. Mansvelder, “Human synapses show a wide temporal window for spike-timing-dependent plasticity,” Front. Synaptic Neurosci. 2, 12 (2010).
[PubMed]

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early Zebrafish Embryos Using Label-Free Nonlinear Microscopy,” Science 329(5994), 967–971 (2010).
[Crossref] [PubMed]

2009 (2)

O. Mărgăritescu, L. Mogoantă, I. Pirici, D. Pirici, D. Cernea, and C. Mărgăritescu, “Histopathological changes in acute ischemic stroke,” Rom. J. Morphol. Embryol. 50(3), 327–339 (2009).
[PubMed]

S. Y. Chen, H. Y. Wu, and C. K. Sun, “In vivo harmonic generation biopsy of human skin,” J. Biomed. Opt. 14(6), 060505 (2009).
[Crossref] [PubMed]

2008 (3)

U. Pichlmeier, A. Bink, G. Schackert, and W. Stummer, “Resection and survival in glioblastoma multiforme: An RTOG recursive partitioning analysis of ALA study patients,” Neuro-oncol. 10(6), 1025–1034 (2008).
[Crossref] [PubMed]

J. S. Smith, E. F. Chang, K. R. Lamborn, S. M. Chang, M. D. Prados, S. Cha, T. Tihan, S. Vandenberg, M. W. McDermott, and M. S. Berger, “Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas,” J. Clin. Oncol. 26(8), 1338–1345 (2008).
[Crossref] [PubMed]

N. Sanai and M. S. Berger, “Glioma extent of resection and its impact on patient outcome,” Neurosurgery 62(4), 753–766 (2008).
[Crossref] [PubMed]

2007 (1)

D. Débarre and E. Beaurepaire, “Quantitative characterization of biological liquids for third-harmonic generation microscopy,” Biophys. J. 92(2), 603–612 (2007).
[Crossref] [PubMed]

2006 (3)

S. Y. Chen, C. S. Hsieh, S. W. Chu, C. Y. Lin, C. Y. Ko, Y. C. Chen, H. J. Tsai, C. H. Hu, and C. K. Sun, “Noninvasive harmonics optical microscopy for long-term observation of embryonic nervous system development in vivo,” J. Biomed. Opt. 11(5), 054022 (2006).
[Crossref] [PubMed]

D. Débarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, “Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy,” Nat. Methods 3(1), 47–53 (2006).
[Crossref] [PubMed]

J. A. Schwartzbaum, J. L. Fisher, K. D. Aldape, and M. Wrensch, “Epidemiology and molecular pathology of glioma,” Nat. Clin. Pract. Neurol. 2(9), 494–516 (2006).
[Crossref] [PubMed]

2005 (2)

N. G. Burnet, S. J. Jefferies, R. J. Benson, D. P. Hunt, and F. P. Treasure, “Years of life lost (YLL) from cancer is an important measure of population burden--and should be considered when allocating research funds,” Br. J. Cancer 92(2), 241–245 (2005).
[PubMed]

S. W. Chu, S. P. Tai, C. L. Ho, C. H. Lin, and C. K. Sun, “High-resolution simultaneous three-photon fluorescence and third-Harmonic-generation microscopy,” Microsc. Res. Tech. 66(4), 193–197 (2005).
[Crossref] [PubMed]

2004 (2)

M. J. Levene, D. A. Dombeck, K. A. Kasischke, R. P. Molloy, and W. W. Webb, “In vivo multiphoton microscopy of deep brain tissue,” J. Neurophysiol. 91(4), 1908–1912 (2004).
[Crossref] [PubMed]

D. Oron, D. Yelin, E. Tal, S. Raz, R. Fachima, and Y. Silberberg, “Depth-resolved structural imaging by third-harmonic generation microscopy,” J. Struct. Biol. 147(1), 3–11 (2004).
[Crossref] [PubMed]

2002 (2)

J. X. Cheng and X. S. Xie, “Green’s function formulation for third-harmonic generation microscopy,” J. Opt. Soc. Am. B 19(7), 1604–1610 (2002).
[Crossref]

I. H. Chen, S. W. Chu, C. K. Sun, P. C. Cheng, and B. L. Lin, “Wavelength dependent damage in biological multi-photon confocal microscopy: A micro-spectroscopic comparison between femtosecond Ti:sapphire and Cr:forsterite laser sources,” Opt. Quantum Electron. 34(12), 1251–1266 (2002).
[Crossref]

2000 (1)

A. Novotny, J. Xiang, W. Stummer, N. S. Teuscher, D. E. Smith, and R. F. Keep, “Mechanisms of 5-aminolevulinic acid uptake at the choroid plexus,” J. Neurochem. 75(1), 321–328 (2000).
[Crossref] [PubMed]

1999 (1)

1998 (2)

M. Müller, J. Squier, K. R. Wilson, and G. J. Brakenhoff, “3D microscopy of transparent objects using third-harmonic generation,” J. Microsc. 191(3), 266–274 (1998).
[Crossref] [PubMed]

J. Squier, M. Muller, G. Brakenhoff, and K. R. Wilson, “Third harmonic generation microscopy,” Opt. Express 3(9), 315–324 (1998).
[Crossref] [PubMed]

1997 (1)

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Adur, J.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, D. B. Almeida, L. A. Andrade, F. Bottcher-Luiz, H. F. Carvalho, and C. L. Cesar, “Optical biomarkers of serous and mucinous human ovarian tumor assessed with nonlinear optics microscopies,” PLoS One 7(10), e47007 (2012).
[Crossref] [PubMed]

Agar, N. Y.

M. Ji, D. A. Orringer, C. W. Freudiger, S. Ramkissoon, X. Liu, D. Lau, A. J. Golby, I. Norton, M. Hayashi, N. Y. Agar, G. S. Young, C. Spino, S. Santagata, S. Camelo-Piragua, K. L. Ligon, O. Sagher, and X. S. Xie, “Rapid, label-free detection of brain tumors with stimulated Raman scattering microscopy,” Sci. Transl. Med. 5(201), 201ra119 (2013).
[Crossref] [PubMed]

Albert, I.

M. Hefti, H. M. Mehdorn, I. Albert, and L. Dorner, “Fluorescence-Guided Surgery for Malignant Glioma: A Review on Aminolevulinic Acid Induced Protoporphyrin IX Photodynamic Diagnostic in Brain Tumors,” Curr. Med. Imaging Rev. 6(4), 254–258 (2010).
[Crossref]

Aldape, K. D.

J. A. Schwartzbaum, J. L. Fisher, K. D. Aldape, and M. Wrensch, “Epidemiology and molecular pathology of glioma,” Nat. Clin. Pract. Neurol. 2(9), 494–516 (2006).
[Crossref] [PubMed]

Almeida, D. B.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, D. B. Almeida, L. A. Andrade, F. Bottcher-Luiz, H. F. Carvalho, and C. L. Cesar, “Optical biomarkers of serous and mucinous human ovarian tumor assessed with nonlinear optics microscopies,” PLoS One 7(10), e47007 (2012).
[Crossref] [PubMed]

Andrade, L. A.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, D. B. Almeida, L. A. Andrade, F. Bottcher-Luiz, H. F. Carvalho, and C. L. Cesar, “Optical biomarkers of serous and mucinous human ovarian tumor assessed with nonlinear optics microscopies,” PLoS One 7(10), e47007 (2012).
[Crossref] [PubMed]

Baayen, J. C.

G. Testa-Silva, M. B. Verhoog, N. A. Goriounova, A. Loebel, J. Hjorth, J. C. Baayen, C. P. J. de Kock, and H. D. Mansvelder, “Human synapses show a wide temporal window for spike-timing-dependent plasticity,” Front. Synaptic Neurosci. 2, 12 (2010).
[PubMed]

Bakker, G.-J.

B. Weigelin, G.-J. Bakker, and P. Friedl, “Intravital third harmonic generation microscopy of collective melanoma cell invasion,” Intra.Vital 1(1), 32–43 (2012).

Barad, Y.

Y. Barad, H. Eisenberg, M. Horowitz, and Y. Silberberg, “Nonlinear scanning laser microscopy by third harmonic generation,” Appl. Phys. Lett. 70(8), 922–924 (1997).
[Crossref]

Baratti, M. O.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, D. B. Almeida, L. A. Andrade, F. Bottcher-Luiz, H. F. Carvalho, and C. L. Cesar, “Optical biomarkers of serous and mucinous human ovarian tumor assessed with nonlinear optics microscopies,” PLoS One 7(10), e47007 (2012).
[Crossref] [PubMed]

Beaurepaire, E.

P. Mahou, N. Olivier, G. Labroille, L. Duloquin, J. M. Sintes, N. Peyriéras, R. Legouis, D. Débarre, and E. Beaurepaire, “Combined third-harmonic generation and four-wave mixing microscopy of tissues and embryos,” Biomed. Opt. Express 2(10), 2837–2849 (2011).
[Crossref] [PubMed]

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early Zebrafish Embryos Using Label-Free Nonlinear Microscopy,” Science 329(5994), 967–971 (2010).
[Crossref] [PubMed]

D. Débarre and E. Beaurepaire, “Quantitative characterization of biological liquids for third-harmonic generation microscopy,” Biophys. J. 92(2), 603–612 (2007).
[Crossref] [PubMed]

D. Débarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, “Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy,” Nat. Methods 3(1), 47–53 (2006).
[Crossref] [PubMed]

Benson, R. J.

N. G. Burnet, S. J. Jefferies, R. J. Benson, D. P. Hunt, and F. P. Treasure, “Years of life lost (YLL) from cancer is an important measure of population burden--and should be considered when allocating research funds,” Br. J. Cancer 92(2), 241–245 (2005).
[PubMed]

Berger, M. S.

J. S. Smith, E. F. Chang, K. R. Lamborn, S. M. Chang, M. D. Prados, S. Cha, T. Tihan, S. Vandenberg, M. W. McDermott, and M. S. Berger, “Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas,” J. Clin. Oncol. 26(8), 1338–1345 (2008).
[Crossref] [PubMed]

N. Sanai and M. S. Berger, “Glioma extent of resection and its impact on patient outcome,” Neurosurgery 62(4), 753–766 (2008).
[Crossref] [PubMed]

Bernstein, L.

M. Jermyn, K. Mok, J. Mercier, J. Desroches, J. Pichette, K. Saint-Arnaud, L. Bernstein, M. C. Guiot, K. Petrecca, and F. Leblond, “Intraoperative brain cancer detection with Raman spectroscopy in humans,” Sci. Transl. Med. 7(274), ra19 (2015).
[Crossref] [PubMed]

Bink, A.

W. Stummer, J. C. Tonn, C. Goetz, W. Ullrich, H. Stepp, A. Bink, T. Pietsch, and U. Pichlmeier, “5-Aminolevulinic Acid-Derived Tumor Fluorescence: The Diagnostic Accuracy of Visible Fluorescence Qualities as Corroborated by Spectrometry and Histology and Postoperative Imaging,” Neurosurgery 74(3), 310–320 (2014).
[Crossref] [PubMed]

U. Pichlmeier, A. Bink, G. Schackert, and W. Stummer, “Resection and survival in glioblastoma multiforme: An RTOG recursive partitioning analysis of ALA study patients,” Neuro-oncol. 10(6), 1025–1034 (2008).
[Crossref] [PubMed]

Bottcher-Luiz, F.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, D. B. Almeida, L. A. Andrade, F. Bottcher-Luiz, H. F. Carvalho, and C. L. Cesar, “Optical biomarkers of serous and mucinous human ovarian tumor assessed with nonlinear optics microscopies,” PLoS One 7(10), e47007 (2012).
[Crossref] [PubMed]

Bourgine, P.

N. Olivier, M. A. Luengo-Oroz, L. Duloquin, E. Faure, T. Savy, I. Veilleux, X. Solinas, D. Débarre, P. Bourgine, A. Santos, N. Peyriéras, and E. Beaurepaire, “Cell Lineage Reconstruction of Early Zebrafish Embryos Using Label-Free Nonlinear Microscopy,” Science 329(5994), 967–971 (2010).
[Crossref] [PubMed]

Brakenhoff, G.

Brakenhoff, G. J.

M. Müller, J. Squier, K. R. Wilson, and G. J. Brakenhoff, “3D microscopy of transparent objects using third-harmonic generation,” J. Microsc. 191(3), 266–274 (1998).
[Crossref] [PubMed]

Brown, C. M.

C. M. Brown, D. R. Rivera, I. Pavlova, D. G. Ouzounov, W. O. Williams, S. Mohanan, W. W. Webb, and C. Xu, “In vivo imaging of unstained tissues using a compact and flexible multiphoton microendoscope,” J. Biomed. Opt. 17(4), 040505 (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]

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]

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]

Buchfelder, M.

I. Y. Eyüpoglu, M. Buchfelder, and N. E. Savaskan, “Surgical resection of malignant gliomas-role in optimizing patient outcome,” Nat. Rev. Neurol. 9(3), 141–151 (2013).
[Crossref] [PubMed]

Burnet, N. G.

N. G. Burnet, S. J. Jefferies, R. J. Benson, D. P. Hunt, and F. P. Treasure, “Years of life lost (YLL) from cancer is an important measure of population burden--and should be considered when allocating research funds,” Br. J. Cancer 92(2), 241–245 (2005).
[PubMed]

Camelo-Piragua, S.

M. Ji, S. Lewis, S. Camelo-Piragua, S. H. Ramkissoon, M. Snuderl, S. Venneti, A. Fisher-Hubbard, M. Garrard, D. Fu, A. C. Wang, J. A. Heth, C. O. Maher, N. Sanai, T. D. Johnson, C. W. Freudiger, O. Sagher, X. S. Xie, and D. A. Orringer, “Detection of human brain tumor infiltration with quantitative stimulated Raman scattering microscopy,” Sci. Transl. Med. 7(309), 309ra163 (2015).
[Crossref] [PubMed]

M. Ji, D. A. Orringer, C. W. Freudiger, S. Ramkissoon, X. Liu, D. Lau, A. J. Golby, I. Norton, M. Hayashi, N. Y. Agar, G. S. Young, C. Spino, S. Santagata, S. Camelo-Piragua, K. L. Ligon, O. Sagher, and X. S. Xie, “Rapid, label-free detection of brain tumors with stimulated Raman scattering microscopy,” Sci. Transl. Med. 5(201), 201ra119 (2013).
[Crossref] [PubMed]

Carvalho, H. F.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, D. B. Almeida, L. A. Andrade, F. Bottcher-Luiz, H. F. Carvalho, and C. L. Cesar, “Optical biomarkers of serous and mucinous human ovarian tumor assessed with nonlinear optics microscopies,” PLoS One 7(10), e47007 (2012).
[Crossref] [PubMed]

Cernea, D.

O. Mărgăritescu, L. Mogoantă, I. Pirici, D. Pirici, D. Cernea, and C. Mărgăritescu, “Histopathological changes in acute ischemic stroke,” Rom. J. Morphol. Embryol. 50(3), 327–339 (2009).
[PubMed]

Cesar, C. L.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, D. B. Almeida, L. A. Andrade, F. Bottcher-Luiz, H. F. Carvalho, and C. L. Cesar, “Optical biomarkers of serous and mucinous human ovarian tumor assessed with nonlinear optics microscopies,” PLoS One 7(10), e47007 (2012).
[Crossref] [PubMed]

Cha, S.

J. S. Smith, E. F. Chang, K. R. Lamborn, S. M. Chang, M. D. Prados, S. Cha, T. Tihan, S. Vandenberg, M. W. McDermott, and M. S. Berger, “Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas,” J. Clin. Oncol. 26(8), 1338–1345 (2008).
[Crossref] [PubMed]

Chaichana, K. L.

C. Kut, K. L. Chaichana, J. Xi, S. M. Raza, X. Ye, E. R. McVeigh, F. J. Rodriguez, A. Quiñones-Hinojosa, and X. Li, “Detection of human brain cancer infiltration ex vivo and in vivo using quantitative optical coherence tomography,” Sci. Transl. Med. 7(292), ra100 (2015).
[Crossref] [PubMed]

Chan, M.-C.

Chang, E. F.

J. S. Smith, E. F. Chang, K. R. Lamborn, S. M. Chang, M. D. Prados, S. Cha, T. Tihan, S. Vandenberg, M. W. McDermott, and M. S. Berger, “Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas,” J. Clin. Oncol. 26(8), 1338–1345 (2008).
[Crossref] [PubMed]

Chang, S. M.

J. S. Smith, E. F. Chang, K. R. Lamborn, S. M. Chang, M. D. Prados, S. Cha, T. Tihan, S. Vandenberg, M. W. McDermott, and M. S. Berger, “Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas,” J. Clin. Oncol. 26(8), 1338–1345 (2008).
[Crossref] [PubMed]

Chen, I. H.

S.-H. Chia, C.-H. Yu, C.-H. Lin, N.-C. Cheng, T.-M. Liu, M.-C. Chan, I. H. Chen, and C.-K. Sun, “Miniaturized video-rate epi-third-harmonic-generation fiber-microscope,” Opt. Express 18(16), 17382–17391 (2010).
[Crossref] [PubMed]

I. H. Chen, S. W. Chu, C. K. Sun, P. C. Cheng, and B. L. Lin, “Wavelength dependent damage in biological multi-photon confocal microscopy: A micro-spectroscopic comparison between femtosecond Ti:sapphire and Cr:forsterite laser sources,” Opt. Quantum Electron. 34(12), 1251–1266 (2002).
[Crossref]

Chen, S. Y.

S. Y. Chen, H. Y. Wu, and C. K. Sun, “In vivo harmonic generation biopsy of human skin,” J. Biomed. Opt. 14(6), 060505 (2009).
[Crossref] [PubMed]

S. Y. Chen, C. S. Hsieh, S. W. Chu, C. Y. Lin, C. Y. Ko, Y. C. Chen, H. J. Tsai, C. H. Hu, and C. K. Sun, “Noninvasive harmonics optical microscopy for long-term observation of embryonic nervous system development in vivo,” J. Biomed. Opt. 11(5), 054022 (2006).
[Crossref] [PubMed]

Chen, Y. C.

S. Y. Chen, C. S. Hsieh, S. W. Chu, C. Y. Lin, C. Y. Ko, Y. C. Chen, H. J. Tsai, C. H. Hu, and C. K. Sun, “Noninvasive harmonics optical microscopy for long-term observation of embryonic nervous system development in vivo,” J. Biomed. Opt. 11(5), 054022 (2006).
[Crossref] [PubMed]

Cheng, J. X.

Cheng, N.-C.

Cheng, P. C.

I. H. Chen, S. W. Chu, C. K. Sun, P. C. Cheng, and B. L. Lin, “Wavelength dependent damage in biological multi-photon confocal microscopy: A micro-spectroscopic comparison between femtosecond Ti:sapphire and Cr:forsterite laser sources,” Opt. Quantum Electron. 34(12), 1251–1266 (2002).
[Crossref]

Chia, S.-H.

Chu, S. W.

S. Y. Chen, C. S. Hsieh, S. W. Chu, C. Y. Lin, C. Y. Ko, Y. C. Chen, H. J. Tsai, C. H. Hu, and C. K. Sun, “Noninvasive harmonics optical microscopy for long-term observation of embryonic nervous system development in vivo,” J. Biomed. Opt. 11(5), 054022 (2006).
[Crossref] [PubMed]

S. W. Chu, S. P. Tai, C. L. Ho, C. H. Lin, and C. K. Sun, “High-resolution simultaneous three-photon fluorescence and third-Harmonic-generation microscopy,” Microsc. Res. Tech. 66(4), 193–197 (2005).
[Crossref] [PubMed]

I. H. Chen, S. W. Chu, C. K. Sun, P. C. Cheng, and B. L. Lin, “Wavelength dependent damage in biological multi-photon confocal microscopy: A micro-spectroscopic comparison between femtosecond Ti:sapphire and Cr:forsterite laser sources,” Opt. Quantum Electron. 34(12), 1251–1266 (2002).
[Crossref]

Clark, C. G.

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[Crossref] [PubMed]

N. G. Horton, K. Wang, D. Kobat, C. G. Clark, F. W. Wise, C. B. Schaffer, and C. Xu, “In vivo three-photon microscopy of subcortical structures within an intact mouse brain,” Nat. Photonics 7(3), 205–209 (2013).
[Crossref] [PubMed]

Cohen-Gadol, A. A.

Y. Li, R. Rey-Dios, D. W. Roberts, P. A. Valdés, and A. A. Cohen-Gadol, “Intraoperative Fluorescence-Guided Resection of High-Grade Gliomas: A Comparison of the Present Techniques and Evolution of Future Strategies,” World. Neurosurg. 82(1-2), 175–185 (2014).
[Crossref] [PubMed]

Combettes, L.

D. Débarre, W. Supatto, A. M. Pena, A. Fabre, T. Tordjmann, L. Combettes, M. C. Schanne-Klein, and E. Beaurepaire, “Imaging lipid bodies in cells and tissues using third-harmonic generation microscopy,” Nat. Methods 3(1), 47–53 (2006).
[Crossref] [PubMed]

de Gooijer, M. C.

O. van Tellingen, B. Yetkin-Arik, M. C. de Gooijer, P. Wesseling, T. Wurdinger, and H. E. de Vries, “Overcoming the blood-brain tumor barrier for effective glioblastoma treatment,” Drug Resist. Updat. 19, 1–12 (2015).
[Crossref] [PubMed]

de Kock, C. P. J.

S. Witte, A. Negrean, J. C. Lodder, C. P. J. de Kock, G. Testa Silva, H. D. Mansvelder, and M. Louise Groot, “Label-free live brain imaging and targeted patching with third-harmonic generation microscopy,” Proc. Natl. Acad. Sci. U.S.A. 108(15), 5970–5975 (2011).
[Crossref] [PubMed]

G. Testa-Silva, M. B. Verhoog, N. A. Goriounova, A. Loebel, J. Hjorth, J. C. Baayen, C. P. J. de Kock, and H. D. Mansvelder, “Human synapses show a wide temporal window for spike-timing-dependent plasticity,” Front. Synaptic Neurosci. 2, 12 (2010).
[PubMed]

de Thomaz, A. A.

J. Adur, V. B. Pelegati, A. A. de Thomaz, M. O. Baratti, D. B. Almeida, L. A. Andrade, F. Bottcher-Luiz, H. F. Carvalho, and C. L. Cesar, “Optical biomarkers of serous and mucinous human ovarian tumor assessed with nonlinear optics microscopies,” PLoS One 7(10), e47007 (2012).
[Crossref] [PubMed]

de Vries, H. E.

O. van Tellingen, B. Yetkin-Arik, M. C. de Gooijer, P. Wesseling, T. Wurdinger, and H. E. de Vries, “Overcoming the blood-brain tumor barrier for effective glioblastoma treatment,” Drug Resist. Updat. 19, 1–12 (2015).
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Débarre, D.

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Wrensch, M.

J. A. Schwartzbaum, J. L. Fisher, K. D. Aldape, and M. Wrensch, “Epidemiology and molecular pathology of glioma,” Nat. Clin. Pract. Neurol. 2(9), 494–516 (2006).
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S. Y. Chen, H. Y. Wu, and C. K. Sun, “In vivo harmonic generation biopsy of human skin,” J. Biomed. Opt. 14(6), 060505 (2009).
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P. C. Wu, T. Y. Hsieh, Z. U. Tsai, and T. M. Liu, “In vivo quantification of the structural changes of collagens in a melanoma microenvironment with second and third harmonic generation microscopy,” Sci. Rep. 5, 8879 (2015).
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Wurdinger, T.

O. van Tellingen, B. Yetkin-Arik, M. C. de Gooijer, P. Wesseling, T. Wurdinger, and H. E. de Vries, “Overcoming the blood-brain tumor barrier for effective glioblastoma treatment,” Drug Resist. Updat. 19, 1–12 (2015).
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C. Kut, K. L. Chaichana, J. Xi, S. M. Raza, X. Ye, E. R. McVeigh, F. J. Rodriguez, A. Quiñones-Hinojosa, and X. Li, “Detection of human brain cancer infiltration ex vivo and in vivo using quantitative optical coherence tomography,” Sci. Transl. Med. 7(292), ra100 (2015).
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A. Novotny, J. Xiang, W. Stummer, N. S. Teuscher, D. E. Smith, and R. F. Keep, “Mechanisms of 5-aminolevulinic acid uptake at the choroid plexus,” J. Neurochem. 75(1), 321–328 (2000).
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M. Ji, S. Lewis, S. Camelo-Piragua, S. H. Ramkissoon, M. Snuderl, S. Venneti, A. Fisher-Hubbard, M. Garrard, D. Fu, A. C. Wang, J. A. Heth, C. O. Maher, N. Sanai, T. D. Johnson, C. W. Freudiger, O. Sagher, X. S. Xie, and D. A. Orringer, “Detection of human brain tumor infiltration with quantitative stimulated Raman scattering microscopy,” Sci. Transl. Med. 7(309), 309ra163 (2015).
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U. Pichlmeier, A. Bink, G. Schackert, and W. Stummer, “Resection and survival in glioblastoma multiforme: An RTOG recursive partitioning analysis of ALA study patients,” Neuro-oncol. 10(6), 1025–1034 (2008).
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H. Lim, D. Sharoukhov, I. Kassim, Y. Zhang, J. L. Salzer, and C. V. Melendez-Vasquez, “Label-free imaging of Schwann cell myelination by third harmonic generation microscopy,” Proc. Natl. Acad. Sci. USA 111(50), 18025–18030 (2014).

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P. C. Wu, T. Y. Hsieh, Z. U. Tsai, and T. M. Liu, “In vivo quantification of the structural changes of collagens in a melanoma microenvironment with second and third harmonic generation microscopy,” Sci. Rep. 5, 8879 (2015).
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Supplementary Material (7)

NameDescription
» Visualization 1: AVI (1653 KB)      A depth scan through the molecular layer of structurally normal human cerebral cortex.
» Visualization 2: AVI (1823 KB)      A depth scan through the pyramidal cell layer of structurally normal human cerebral cortex.
» Visualization 3: AVI (436 KB)      A depth scan through white matter of structurally normal human brain tissue.
» Visualization 4: AVI (2393 KB)      2D inspection mode THG/SHG imaging of a low-grade oligodendroglioma sample.
» Visualization 5: AVI (2591 KB)      2D inspection mode THG/SHG imaging of a high-grade glioma (glioblastoma) sample.
» Visualization 6: AVI (298 KB)      A depth scan through the transition zone between a low-grade glioma and normal human brain tissue.
» Visualization 7: AVI (647 KB)      A depth scan through an area of high cellularity in a low-grade glioma sample.

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Figures (10)

Fig. 1
Fig. 1 THG/SHG microscopy for brain tissue imaging. (A) Energy level diagram of the second (SHG) and third (THG) harmonic generation process. (B) Energy level diagram of the two- (2PF) and three-photon (3PF) excited auto-fluorescence process. (C) Multiphoton microscope setup: Laser producing 200 fs pulses at 1200 nm; GM – X-Y galvo-scanner mirrors; SL – scan lens; TL – tube lens; MO – microscope objective; DM1 – dichroic mirror reflecting back-scattered THG/SHG photons to the PMT detectors; DM2 – dichroic mirror splitting SHG and THG channels; F – narrow-band SHG and THG interference filters; L – focusing lenses; PMT – photomultiplier tube detectors. (D) Infrared photons (white arrow) are focused deep in the brain tissue, converted to THG (green) and SHG (red) photons, scattered back (green/red arrows) and epi-detected. The nonlinear optical processes result in label-free contrast images with sub-cellular resolution and intrinsic depth sectioning. (E and F) Freshly-excised low-grade (E) and high-grade (F) glioma tissue samples in artificial cerebrospinal fluid (ACSF) in a Petri dish with a millimeter paper underneath for scale. (G) An agar-embedded tumor tissue sample under 0.17 mm glass cover slip with the microscope objective (MO) on top.
Fig. 2
Fig. 2 Structurally normal human brain tissue. (A) THG (green) and SHG (red) image of 1.80 × 4.95 mm2 ex-vivo, structurally normal, fresh human neocortex and subcortical white matter tissue. (B) Myelin-stained histology image of a similar region of the brain. Key tissue components marked with white squares are shown enlarged in the right panels, together with histology images; molecular layer (C, D); large pyramidal neurons layer (E, F); white matter (G, H); a capillary blood vessel with intraluminal erythrocytes (I, J). The stain in panels (B, D, F, H) is luxol fast blue (LFB) to reveal myelin, and hemotoxin-and-eosion (H&E) in (J). Images C, E and G are composed of single 2-μm-thick optical sections, imaging time 1.2 s. Image I is composed of 21 images taken with 2-μm steps over 40 μm depth, imaging time 1.5 min. The inset of image I shows a cross-section of the capillary along the white line, revealing a round contour of this microvessel (SHG) and corroborating the intraluminal position of the erythrocytes (THG).
Fig. 3
Fig. 3 Infiltrative low-grade glioma: transition zone. (A–D) THG/SHG images of the low-to-high cellularity transition zone in a tissue sample diagnosed by the neuropathologist as diffuse low-grade oligodendroglioma on the basis of H&E-stained histological sections. (A) Mosaic image of the transition zone in the white matter. Image is composed of 3 × 2 = 6 tiles, 1.35 × 0.90 mm2, each tile 450 × 450 μm2, 1000 × 1000 pixels2, total imaging time 52 sec. (B–D) Magnified low- (B), intermediate- (C) and high-cellularity (D) areas marked on the image (A) with white squares. Images (B, C) show 2-μm-thick optical sections taken at depths of 20–30 μm with acquisition time of 0.6 s. (E to H) H&E images of the sample areas corresponding to the THG/SHG images: A–E, B–F, C–G, D–H.
Fig. 4
Fig. 4 Infiltrative low-grade glioma: mixed cellularity area. (A) Mosaic image of brain tumor area with spatially varying cellular density. Image is composed of single images (tiles) with boundaries indicated by dotted white lines, each tile is 400 × 400 μm2, 254 × 254 pixels2. Each tile shows a single optical section about 2-μm thick and taken at a depth of 20–30 μm. Mosaic size: 11 × 8 = 88 tiles; imaged area: 4.4 × 3.2 mm2; total imaging time: 3.7 min. (B,C) Magnified images of the low- (B) and increased cellularity (C) areas indicated on the image (A). Images (B,C) show single optical sections about 2-μm thick taken at depths of 20–30 μm with an acquisition time of 5 s.
Fig. 5
Fig. 5 High-grade glioma in the white matter. Combined THG/SHG images of the focus of a high-grade glioma with high cellularity and intense vascular proliferation. (A) Mosaic image composed of single tiles, each tile 450 × 450 μm2, 517 × 517 pixels2, each tile showing a single 2-μm-thick optical section taken at a depth of 20–30 μm. Mosaic size 4 × 3 = 24 tiles; imaged area 1.80 × 1.35 mm2; total imaging time 1.5 min. (B and C) Magnified images of the areas containing smaller (B) and larger (C) blood vessels. Images (B and C) show single 2-μm-thick optical sections taken at depths of 20–30 μm with an acquisition time of 8 s. H&E histology of the HGG sample is shown in Fig. 7.
Fig. 6
Fig. 6 High-grade glioma: peritumoral neocortex tissue with secondary changes. (A) Mosaic image is composed of 450 × 450 μm2 tiles, 517 × 517 pixels2, each tile showing a single 2-μm-thick optical section taken at a depth of 20–30 μm. Mosaic size 5 × 4 = 20 tiles; imaged area 2.25 × 1.80 mm2; total imaging time 1.7 min. (B and C) Magnified image of a tumor cell lesion (B) and an area with bright cells (black round holes are cells’ nuclei) and a blood vessel (C). Images (B and C) show single 2-μm-thick optical sections taken at depths of 20–30 μm, acquisition times 15 s (B) and 8 s (C).
Fig. 7
Fig. 7 Various cytological and histological features observed with THG/SHG imaging modalities in low- and high-grade glioma tissues. Label-free images of 2-μm-thick optical sections taken at depths of 20–30 μm with acquisition times of 0.5–5 s and H&E images of corresponding tissue areas. (A, B) Glial cell with a nearly round nucleus and large nuclear/cytoplasm ratio. (C, D) Glial cell with a round nucleus and smaller nuclear/cytoplasm ratio. (E, F) Glial cell with an indented nucleus and multiple nucleoli. (G, H) Highly cellular area in high-grade glioma (glioblastoma) with multiple pleomorphic tumor cell nuclei with dense chromatin and high nuclear/cytoplasmatic ratio. (I, J) A neuronal or glial cell with vacuolated cytoplasm in the edematic peritumoral neocortex of the high-grade glioma tissue. Autofluorescent deposits in the neuropil appear as yellow dots. (K, L) Corpus amylaceum surrounded by neuropil. (M, N) Intense vascular proliferation in high-grade glioma focus.
Fig. 8
Fig. 8 THG imaging for different brain tissues types at varying depths. (A) Horizontal THG intensity profile was taken over a mosaic image of a white-to-gray matter transition of structurally normal human brain tissue. The mosaic was imaged at a depth of 10–20 μm. As the myelinated fiber density increases from gray matter (GM) to white matter (WM), the THG signal intensity increases by a factor 4. (B) Histogram showing averaged THG signal intensities obtained from THG images collected at depths of 2–4 μm from structurally normal brain WM and GM areas, compared to low-grade glioma areas of WM with low (T1) and high (T2) cell densities and high-grade glioma area (T3) with high cell density. Overall, THG signal intensity increases by factor 17 from T3 to WM. (C to G) THG intensity depth profiles of WM, GM, T1, T2 and T3 areas. THG intensity points (triangles) are obtained by averaging 270 × 270 μm2 images taken every 10 μm down to 300 μm. Solid lines present exponential decay fits: ITHG (z) = I(0) exp(–z/le), where le denotes the THG effective attenuation length, ITHG(le) = 0.37 ITHG(0).
Fig. 9
Fig. 9 Endomicroscopic THG/SHG brain tissue imaging. (A) A sketch of the multiphoton microscope equipped with the micro-objective lens. CL – coupling lens. (B and C) Characterization of the lateral and axial resolution of the micro-objective lens. (B) Lateral (x) and axial (z) resolution of the micro-objective lens measured with fluorescent microspheres via two- and three-photon fluorescence (2P, 3P). Line intensity profiles are taken over the lateral (x) and axial (z) images of the 2P/3P fluorescent spheres and are indicated on the inset image with the white dashed lines. Normalized intensity profile points (open and filled circles and squares) are fitted with Gaussian functions (solid lines) and the values of the full-width-at-half-maximum (FWHM) peak widths are measured. (C) Lateral (x) and axial (z) THG resolution of the micro-objective lens measured with a glass-water interface. The inset images show the lateral (x) and axial (z) THG images of the glass-water interface. THG intensity profiles are measured along the white dashed lines indicated on the inset images. The normalized axial (z) intensity profile points (blue filled triangles) are fitted with Gaussian function (solid blue line) and the FWHM was measured to provide the axial THG resolution. The normalized lateral (x) intensity profile points (open teal triangles) are fitted to the error function (dashed teal line), Erf(x) = A1 + 0.5(A2A1) × [1 – erf(A3x)] with fitting parameters A1 = 0.00 ± 0.01, A2 = 1.00 ± 0.01, and A3 = 1.90 ± 0.08. The lateral THG resolution was measured as the FWHM of the first derivative dErf(x) of the Erf(x) (solid magenta line).
Fig. 10
Fig. 10 THG/SHG endomicroscopy of ex-vivo human brain tissues. SHG (red) and THG (green) images of healthy and tumor-invaded ex-vivo human brain tissue obtained with the micro-objective lens. Each image is a single 4-μm-thick optical section taken at a depth of 20–30 μm below the tissue surface with acquisition time of 16 s and laser power of 50 mW. (A–C) Healthy ex-vivo human brain tissue: gray matter neuropil with neuronal somata with lipofuscin content (yellow) (A) and (B); (C) low-cellularity white matter area. (D) High-grade glioma focus.

Tables (1)

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Table 1 Pre-operative diagnoses and cell densities observed in the studied brain tissue samples by THG imaging and corresponding H&E histopathology.

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