Abstract

Visual guidance at the cellular level during neurosurgical procedures is essential for complete tumour resection. We present a compact reflectance confocal microscope with a 20 mm working distance that provided <1.2 µm spatial resolution over a 600 µm × 600 µm field of view in the near-infrared region. A physical footprint of 200 mm × 550 mm was achieved using only standard off-the-shelf components. Theoretical performance of the optical design was first evaluated via commercial Zemax software. Then three specimens from rodents: fixed brain, frozen calvaria and live hippocampal slices, were used to experimentally assess system capability and robustness. Results show great potential for the proposed system to be translated into use as a next generation label-free and contactless neurosurgical microscope.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2020 (2)

A. Alfonso-Garcia, J. Bec, S. S. Weaver, B. Hartl, J. Unger, M. Bobinski, M. Lechpammer, F. Girgis, J. Boggan, and L. Marcu, “Real-time augmented reality for delineation of surgical margins during neurosurgery using autofluorescence lifetime contrast,” J. Biophotonics 13(1), 108 (2020).
[Crossref]

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[Crossref]

2019 (5)

P. Charalampaki, M. Nakamura, D. Athanasopoulos, and A. Heimann, “Confocal-assisted multispectral fluorescent microscopy for brain tumor surgery,” Front. Oncol. 9, 583 (2019).
[Crossref]

N. Lakomkin and C. G. Hadjipanayis, “The use of spectroscopy handheld tools in brain tumor surgery: Current evidence and techniques,” Front. Surg. 6, 30 (2019).
[Crossref]

D. Y. Zhang, S. Singhal, and J. Y. K. Lee, “Optical principles of fluorescence-guided brain tumor surgery: A practical primer for the neurosurgeon,” Neurosurg. 85(3), 312–324 (2019).
[Crossref]

R. Benavides-Piccione, M. Regalado-Reyes, I. Fernaud-Espinosa, A. Kastanauskaite, S. Tapia-González, G. León-Espinosa, C. Rojo, R. Insausti, I. Segev, and J. DeFelipe, “Differential structure of hippocampal CA1 pyramidal neurons in the human and mouse,” Cereb. Cortex 30(2), 730–752 (2019).
[Crossref]

J. Zhu, S. P. Chong, W. Zhou, and V. J. Srinivasan, “Noninvasive, in vivo rodent brain optical coherence tomography at 2.1 microns,” Opt. Lett. 44(17), 4147–4150 (2019).
[Crossref]

2018 (6)

2017 (6)

C. Cheyuo, W. Grand, and L. L. Balos, “Near-infrared confocal laser reflectance cytoarchitectural imaging of the substantia nigra and cerebellum in the fresh human cadaver,” World Neurosurg. 97, 465–470 (2017).
[Crossref]

N. Ji, “Adaptive optical fluorescence microscopy,” Nat. Methods 14(4), 374–380 (2017).
[Crossref]

J. M. Eschbacher, J. F. Georges, E. Belykh, M. I. Yazdanabadi, N. L. Martirosyan, E. Szeto, C. Y. Seiler, M. A. Mooney, J. K. Daniels, K. Y. Goehring, K. R. Van Keuren-Jensen, M. C. Preul, S. W. Coons, S. Mehta, and P. Nakaji, “Immediate label-free ex vivo evaluation of human brain tumor biopsies with confocal reflectance microscopy,” J. Neuropathol. & Exp. Neurol. 76(12), 1008–1022 (2017).
[Crossref]

M. Žurauskas, O. Barnstedt, M. Frade-Rodriguez, S. Waddell, and M. J. Booth, “Rapid adaptive remote focusing microscope for sensing of volumetric neural activity,” Biomed. Opt. Express 8(10), 4369–4379 (2017).
[Crossref]

X. Tao, T. Lam, B. Zhu, Q. Li, M. R. Reinig, and J. Kubby, “Three-dimensional focusing through scattering media using conjugate adaptive optics with remote focusing (CAORF),” Opt. Express 25(9), 10368–10383 (2017).
[Crossref]

R. Turcotte, Y. Liang, and N. Ji, “Adaptive optical versus spherical aberration corrections for in vivo brain imaging,” Biomed. Opt. Express 8(8), 3891–3902 (2017).
[Crossref]

2016 (2)

N. L. Martirosyan, J. M. Eschbacher, M. Y. S. Kalani, J. D. Turner, E. Belykh, R. F. Spetzler, P. Nakaji, and M. C. Preul, “Prospective evaluation of the utility of intraoperative confocal laser endomicroscopy in patients with brain neoplasms using fluorescein sodium: experience with 74 cases,” Neurosurg. Focus. 40(3), E11 (2016).
[Crossref]

E. Belykh, N. L. Martirosyan, K. Yagmurlu, E. J. Miller, J. M. Eschbacher, M. Izadyyazdanabadi, L. A. Bardonova, V. A. Byvaltsev, P. Nakaji, and M. C. Preul, “Intraoperative fluorescence imaging for personalized brain tumor resection: Current state and future directions,” Front. Surg. 3, 55 (2016).
[Crossref]

2015 (3)

2014 (3)

R. Turcotte, C. Alt, L. J. Mortensen, and C. P. Lin, “Characterization of multiphoton microscopy in the bone marrow following intravital laser osteotomy,” Biomed. Opt. Express 5(10), 3578–3588 (2014).
[Crossref]

A. J. Schain, R. A. Hill, and J. Grutzendler, “Label-free in vivo imaging of myelinated axons in health and disease with spectral confocal reflectance microscopy,” Nat. Med. 20(4), 443–449 (2014).
[Crossref]

K. Erkmen, K. Bekelis, N. E. Simmons, P. A. Valdes, D. W. Roberts, K. D. Paulsen, F. Leblond, B. T. Harris, A. Kim, and B. C. Wilson, “5-aminolevulinic acid-induced protoporphyrin IX fluorescence in meningioma: Qualitative and quantitative measurements in vivo,” Oper. Neurosurg. 10(1), 74–83 (2014).
[Crossref]

2013 (6)

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C.-S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
[Crossref]

A. Grosche, J. Grosche, M. Tackenberg, D. Scheller, G. Gerstner, A. Gumprecht, T. Pannicke, P. G. Hirrlinger, U. Wilhelmsson, and K. Hüttmann, “Versatile and simple approach to determine astrocyte territories in mouse neocortex and hippocampus,” PLoS One 8(7), e69143 (2013).
[Crossref]

C. Leahy, H. Radhakrishnan, and V. J. Srinivasan, “Volumetric imaging and quantification of cytoarchitecture and myeloarchitecture with intrinsic scattering contrast,” Biomed. Opt. Express 4(10), 1978–1990 (2013).
[Crossref]

O. Assayag, K. Grieve, B. Devaux, F. Harms, J. Pallud, F. Chretien, C. Boccara, and P. Varlet, “Imaging of non-tumorous and tumorous human brain tissues with full-field optical coherence tomography,” NeuroImage: Clin. 2, 549–557 (2013).
[Crossref]

L. J. Steven, “Optical properties of biological tissues: a review,” Phys. Med. Biol. 58(11), R37–R61 (2013).
[Crossref]

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. H. van de Velde, and J. V. Frangioni, “Image-guided cancer surgery using near-infrared fluorescence,” Nat. Rev. Clin. Oncol. 10(9), 507–518 (2013).
[Crossref]

2012 (3)

C. Glazowski and M. Rajadhyaksha, “Optimal detection pinhole for lowering speckle noise while maintaining adequate optical sectioning in confocal reflectance microscopes,” J. Biomed. Opt. 17(8), 085001 (2012).
[Crossref]

V. J. Srinivasan, H. Radhakrishnan, J. Y. Jiang, S. Barry, and A. E. Cable, “Optical coherence microscopy for deep tissue imaging of the cerebral cortex with intrinsic contrast,” Opt. Express 20(3), 2220–2239 (2012).
[Crossref]

K. Suto, K. Urabe, K. Naruse, K. Uchida, T. Matsuura, Y. Mikuni-Takagaki, M. Suto, N. Nemoto, K. Kamiya, and M. Itoman, “Repeated freeze-thaw cycles reduce the survival rate of osteocytes in bone-tendon constructs without affecting the mechanical properties of tendons,” Cell Tissue Banking 13(1), 71–80 (2012).
[Crossref]

2011 (1)

J. Ben Arous, J. Binding, J.-F. Leger, M. Casado, P. Topilko, L. Bourdieu, S. Gigan, and A. C. Boccara, “Single myelin fiber imaging in living rodents without labeling by deep optical coherence microscopy,” J. Biomed. Opt. 16(11), 116012 (2011).
[Crossref]

2010 (1)

T. Sankar, P. M. Delaney, R. W. Ryan, J. Eschbacher, M. Abdelwahab, P. Nakaji, S. W. Coons, A. C. Scheck, K. A. Smith, R. F. Spetzler, and M. C. Preul, “Miniaturized handheld confocal microscopy for neurosurgery results in an experimental glioblastoma model,” Neurosurg. 66(2), 410–418 (2010).
[Crossref]

2008 (1)

J.-C. Tonn and W. Stummer, “Fluorescence-guided resection of malignant gliomas using 5-aminolevulinic acid: practical use, risks, and pitfalls,” Clin. Neurosurg. 55, 20–26 (2008).

2007 (1)

J. Booth Martin, “Adaptive optics in microscopy,” Philos. Trans. R. Soc., A 365(1861), 2829–2843 (2007).
[Crossref]

2006 (1)

W. Stummer, U. Pichlmeier, T. Meinel, O. D. Wiestler, F. Zanella, and H.-J. Reulen, “Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial,” The Lancet Oncol. 7(5), 392–401 (2006).
[Crossref]

2005 (1)

Y. Ohno, “Spectral design considerations for white LED color rendering,” Opt. Eng. 44(11), 111302 (2005).
[Crossref]

Abdelwahab, M.

T. Sankar, P. M. Delaney, R. W. Ryan, J. Eschbacher, M. Abdelwahab, P. Nakaji, S. W. Coons, A. C. Scheck, K. A. Smith, R. F. Spetzler, and M. C. Preul, “Miniaturized handheld confocal microscopy for neurosurgery results in an experimental glioblastoma model,” Neurosurg. 66(2), 410–418 (2010).
[Crossref]

Alfonso-Garcia, A.

A. Alfonso-Garcia, J. Bec, S. S. Weaver, B. Hartl, J. Unger, M. Bobinski, M. Lechpammer, F. Girgis, J. Boggan, and L. Marcu, “Real-time augmented reality for delineation of surgical margins during neurosurgery using autofluorescence lifetime contrast,” J. Biophotonics 13(1), 108 (2020).
[Crossref]

Allegra Mascaro, A. L.

Alt, C.

Ancukiewicz, M.

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C.-S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
[Crossref]

Andreana, M.

Assayag, O.

O. Assayag, K. Grieve, B. Devaux, F. Harms, J. Pallud, F. Chretien, C. Boccara, and P. Varlet, “Imaging of non-tumorous and tumorous human brain tissues with full-field optical coherence tomography,” NeuroImage: Clin. 2, 549–557 (2013).
[Crossref]

Athanasopoulos, D.

P. Charalampaki, M. Nakamura, D. Athanasopoulos, and A. Heimann, “Confocal-assisted multispectral fluorescent microscopy for brain tumor surgery,” Front. Oncol. 9, 583 (2019).
[Crossref]

Balos, L. L.

C. Cheyuo, W. Grand, and L. L. Balos, “Near-infrared confocal laser reflectance cytoarchitectural imaging of the substantia nigra and cerebellum in the fresh human cadaver,” World Neurosurg. 97, 465–470 (2017).
[Crossref]

Bardonova, L. A.

E. Belykh, N. L. Martirosyan, K. Yagmurlu, E. J. Miller, J. M. Eschbacher, M. Izadyyazdanabadi, L. A. Bardonova, V. A. Byvaltsev, P. Nakaji, and M. C. Preul, “Intraoperative fluorescence imaging for personalized brain tumor resection: Current state and future directions,” Front. Surg. 3, 55 (2016).
[Crossref]

Barnstedt, O.

Barry, S.

Bec, J.

A. Alfonso-Garcia, J. Bec, S. S. Weaver, B. Hartl, J. Unger, M. Bobinski, M. Lechpammer, F. Girgis, J. Boggan, and L. Marcu, “Real-time augmented reality for delineation of surgical margins during neurosurgery using autofluorescence lifetime contrast,” J. Biophotonics 13(1), 108 (2020).
[Crossref]

Bekelis, K.

K. Erkmen, K. Bekelis, N. E. Simmons, P. A. Valdes, D. W. Roberts, K. D. Paulsen, F. Leblond, B. T. Harris, A. Kim, and B. C. Wilson, “5-aminolevulinic acid-induced protoporphyrin IX fluorescence in meningioma: Qualitative and quantitative measurements in vivo,” Oper. Neurosurg. 10(1), 74–83 (2014).
[Crossref]

Belykh, E.

E. Belykh, A. A. Patel, E. J. Miller, B. Bozkurt, K. Yaǧmurlu, E. C. Woolf, A. C. Scheck, J. M. Eschbacher, P. Nakaji, and M. C. Preul, “Probe-based three-dimensional confocal laser endomicroscopy of brain tumors: technical note,” Cancer Manage. Res. 10, 3109–3123 (2018).
[Crossref]

J. M. Eschbacher, J. F. Georges, E. Belykh, M. I. Yazdanabadi, N. L. Martirosyan, E. Szeto, C. Y. Seiler, M. A. Mooney, J. K. Daniels, K. Y. Goehring, K. R. Van Keuren-Jensen, M. C. Preul, S. W. Coons, S. Mehta, and P. Nakaji, “Immediate label-free ex vivo evaluation of human brain tumor biopsies with confocal reflectance microscopy,” J. Neuropathol. & Exp. Neurol. 76(12), 1008–1022 (2017).
[Crossref]

E. Belykh, N. L. Martirosyan, K. Yagmurlu, E. J. Miller, J. M. Eschbacher, M. Izadyyazdanabadi, L. A. Bardonova, V. A. Byvaltsev, P. Nakaji, and M. C. Preul, “Intraoperative fluorescence imaging for personalized brain tumor resection: Current state and future directions,” Front. Surg. 3, 55 (2016).
[Crossref]

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J. Ben Arous, J. Binding, J.-F. Leger, M. Casado, P. Topilko, L. Bourdieu, S. Gigan, and A. C. Boccara, “Single myelin fiber imaging in living rodents without labeling by deep optical coherence microscopy,” J. Biomed. Opt. 16(11), 116012 (2011).
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E. Belykh, A. A. Patel, E. J. Miller, B. Bozkurt, K. Yaǧmurlu, E. C. Woolf, A. C. Scheck, J. M. Eschbacher, P. Nakaji, and M. C. Preul, “Probe-based three-dimensional confocal laser endomicroscopy of brain tumors: technical note,” Cancer Manage. Res. 10, 3109–3123 (2018).
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K. Erkmen, K. Bekelis, N. E. Simmons, P. A. Valdes, D. W. Roberts, K. D. Paulsen, F. Leblond, B. T. Harris, A. Kim, and B. C. Wilson, “5-aminolevulinic acid-induced protoporphyrin IX fluorescence in meningioma: Qualitative and quantitative measurements in vivo,” Oper. Neurosurg. 10(1), 74–83 (2014).
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A. Alfonso-Garcia, J. Bec, S. S. Weaver, B. Hartl, J. Unger, M. Bobinski, M. Lechpammer, F. Girgis, J. Boggan, and L. Marcu, “Real-time augmented reality for delineation of surgical margins during neurosurgery using autofluorescence lifetime contrast,” J. Biophotonics 13(1), 108 (2020).
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K. Suto, K. Urabe, K. Naruse, K. Uchida, T. Matsuura, Y. Mikuni-Takagaki, M. Suto, N. Nemoto, K. Kamiya, and M. Itoman, “Repeated freeze-thaw cycles reduce the survival rate of osteocytes in bone-tendon constructs without affecting the mechanical properties of tendons,” Cell Tissue Banking 13(1), 71–80 (2012).
[Crossref]

Vahrmeijer, A. L.

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. H. van de Velde, and J. V. Frangioni, “Image-guided cancer surgery using near-infrared fluorescence,” Nat. Rev. Clin. Oncol. 10(9), 507–518 (2013).
[Crossref]

Vajzovic, L.

Valdes, P. A.

K. Erkmen, K. Bekelis, N. E. Simmons, P. A. Valdes, D. W. Roberts, K. D. Paulsen, F. Leblond, B. T. Harris, A. Kim, and B. C. Wilson, “5-aminolevulinic acid-induced protoporphyrin IX fluorescence in meningioma: Qualitative and quantitative measurements in vivo,” Oper. Neurosurg. 10(1), 74–83 (2014).
[Crossref]

van de Velde, C. J. H.

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. H. van de Velde, and J. V. Frangioni, “Image-guided cancer surgery using near-infrared fluorescence,” Nat. Rev. Clin. Oncol. 10(9), 507–518 (2013).
[Crossref]

van der Vorst, J. R.

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. H. van de Velde, and J. V. Frangioni, “Image-guided cancer surgery using near-infrared fluorescence,” Nat. Rev. Clin. Oncol. 10(9), 507–518 (2013).
[Crossref]

Van Keuren-Jensen, K. R.

J. M. Eschbacher, J. F. Georges, E. Belykh, M. I. Yazdanabadi, N. L. Martirosyan, E. Szeto, C. Y. Seiler, M. A. Mooney, J. K. Daniels, K. Y. Goehring, K. R. Van Keuren-Jensen, M. C. Preul, S. W. Coons, S. Mehta, and P. Nakaji, “Immediate label-free ex vivo evaluation of human brain tumor biopsies with confocal reflectance microscopy,” J. Neuropathol. & Exp. Neurol. 76(12), 1008–1022 (2017).
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Varlet, P.

O. Assayag, K. Grieve, B. Devaux, F. Harms, J. Pallud, F. Chretien, C. Boccara, and P. Varlet, “Imaging of non-tumorous and tumorous human brain tissues with full-field optical coherence tomography,” NeuroImage: Clin. 2, 549–557 (2013).
[Crossref]

Vassal, F.

F. Forest, E. Cinotti, V. Yvorel, C. Habougit, F. Vassal, C. Nuti, J.-L. Perrot, B. Labeille, and M. Péoc’h, “Ex vivo confocal microscopy imaging to identify tumor tissue on freshly removed brain sample,” J. Neuro-Oncol. 124(2), 157–164 (2015).
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Vavilin, A.

Waddell, S.

Waterman, G.

Weaver, S. S.

A. Alfonso-Garcia, J. Bec, S. S. Weaver, B. Hartl, J. Unger, M. Bobinski, M. Lechpammer, F. Girgis, J. Boggan, and L. Marcu, “Real-time augmented reality for delineation of surgical margins during neurosurgery using autofluorescence lifetime contrast,” J. Biophotonics 13(1), 108 (2020).
[Crossref]

Widhalm, G.

Wiestler, O. D.

W. Stummer, U. Pichlmeier, T. Meinel, O. D. Wiestler, F. Zanella, and H.-J. Reulen, “Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial,” The Lancet Oncol. 7(5), 392–401 (2006).
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Wilhelmsson, U.

A. Grosche, J. Grosche, M. Tackenberg, D. Scheller, G. Gerstner, A. Gumprecht, T. Pannicke, P. G. Hirrlinger, U. Wilhelmsson, and K. Hüttmann, “Versatile and simple approach to determine astrocyte territories in mouse neocortex and hippocampus,” PLoS One 8(7), e69143 (2013).
[Crossref]

Wilson, B. C.

K. Erkmen, K. Bekelis, N. E. Simmons, P. A. Valdes, D. W. Roberts, K. D. Paulsen, F. Leblond, B. T. Harris, A. Kim, and B. C. Wilson, “5-aminolevulinic acid-induced protoporphyrin IX fluorescence in meningioma: Qualitative and quantitative measurements in vivo,” Oper. Neurosurg. 10(1), 74–83 (2014).
[Crossref]

Wilzbach, M.

Wirth, D.

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C.-S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
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Woolf, E. C.

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Wu, C.

Xia, F.

Xu, C.

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[Crossref]

Yaroslavsky, A. N.

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C.-S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
[Crossref]

Yazdanabadi, M. I.

J. M. Eschbacher, J. F. Georges, E. Belykh, M. I. Yazdanabadi, N. L. Martirosyan, E. Szeto, C. Y. Seiler, M. A. Mooney, J. K. Daniels, K. Y. Goehring, K. R. Van Keuren-Jensen, M. C. Preul, S. W. Coons, S. Mehta, and P. Nakaji, “Immediate label-free ex vivo evaluation of human brain tumor biopsies with confocal reflectance microscopy,” J. Neuropathol. & Exp. Neurol. 76(12), 1008–1022 (2017).
[Crossref]

Yvorel, V.

F. Forest, E. Cinotti, V. Yvorel, C. Habougit, F. Vassal, C. Nuti, J.-L. Perrot, B. Labeille, and M. Péoc’h, “Ex vivo confocal microscopy imaging to identify tumor tissue on freshly removed brain sample,” J. Neuro-Oncol. 124(2), 157–164 (2015).
[Crossref]

Zanella, F.

W. Stummer, U. Pichlmeier, T. Meinel, O. D. Wiestler, F. Zanella, and H.-J. Reulen, “Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial,” The Lancet Oncol. 7(5), 392–401 (2006).
[Crossref]

Zhang, D. Y.

D. Y. Zhang, S. Singhal, and J. Y. K. Lee, “Optical principles of fluorescence-guided brain tumor surgery: A practical primer for the neurosurgeon,” Neurosurg. 85(3), 312–324 (2019).
[Crossref]

Zhou, W.

Zhu, B.

Zhu, J.

Žurauskas, M.

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C. Leahy, H. Radhakrishnan, and V. J. Srinivasan, “Volumetric imaging and quantification of cytoarchitecture and myeloarchitecture with intrinsic scattering contrast,” Biomed. Opt. Express 4(10), 1978–1990 (2013).
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R. Turcotte, Y. Liang, and N. Ji, “Adaptive optical versus spherical aberration corrections for in vivo brain imaging,” Biomed. Opt. Express 8(8), 3891–3902 (2017).
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M. Žurauskas, O. Barnstedt, M. Frade-Rodriguez, S. Waddell, and M. J. Booth, “Rapid adaptive remote focusing microscope for sensing of volumetric neural activity,” Biomed. Opt. Express 8(10), 4369–4379 (2017).
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J. Cha, A. Broch, S. Mudge, K. Kim, J.-M. Namgoong, E. Oh, and P. Kim, “Real-time, label-free, intraoperative visualization of peripheral nerves and micro-vasculatures using multimodal optical imaging techniques,” Biomed. Opt. Express 9(3), 1097–1110 (2018).
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F. Xia, C. Wu, D. Sinefeld, B. Li, Y. Qin, and C. Xu, “In vivo label-free confocal imaging of the deep mouse brain with long-wavelength illumination,” Biomed. Opt. Express 9(12), 6545–6555 (2018).
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D. Reichert, M. T. Erkkilä, G. Holst, N. Hecker-Denschlag, M. Wilzbach, C. Hauger, W. Drexler, J. Gesperger, B. Kiesel, T. Roetzer, A. Unterhuber, G. Widhalm, R. A. Leitgeb, and M. Andreana, “Towards real-time wide-field fluorescence lifetime imaging of 5-ALA labeled brain tumors with multi-tap CMOS cameras,” Biomed. Opt. Express 11(3), 1598–1616 (2020).
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Brain Pathol. (1)

M. Snuderl, D. Wirth, S. A. Sheth, S. K. Bourne, C.-S. Kwon, M. Ancukiewicz, W. T. Curry, M. P. Frosch, and A. N. Yaroslavsky, “Dye-enhanced multimodal confocal imaging as a novel approach to intraoperative diagnosis of brain tumors,” Brain Pathol. 23(1), 73–81 (2013).
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Cancer Manage. Res. (1)

E. Belykh, A. A. Patel, E. J. Miller, B. Bozkurt, K. Yaǧmurlu, E. C. Woolf, A. C. Scheck, J. M. Eschbacher, P. Nakaji, and M. C. Preul, “Probe-based three-dimensional confocal laser endomicroscopy of brain tumors: technical note,” Cancer Manage. Res. 10, 3109–3123 (2018).
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Cell Tissue Banking (1)

K. Suto, K. Urabe, K. Naruse, K. Uchida, T. Matsuura, Y. Mikuni-Takagaki, M. Suto, N. Nemoto, K. Kamiya, and M. Itoman, “Repeated freeze-thaw cycles reduce the survival rate of osteocytes in bone-tendon constructs without affecting the mechanical properties of tendons,” Cell Tissue Banking 13(1), 71–80 (2012).
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Cereb. Cortex (1)

R. Benavides-Piccione, M. Regalado-Reyes, I. Fernaud-Espinosa, A. Kastanauskaite, S. Tapia-González, G. León-Espinosa, C. Rojo, R. Insausti, I. Segev, and J. DeFelipe, “Differential structure of hippocampal CA1 pyramidal neurons in the human and mouse,” Cereb. Cortex 30(2), 730–752 (2019).
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J.-C. Tonn and W. Stummer, “Fluorescence-guided resection of malignant gliomas using 5-aminolevulinic acid: practical use, risks, and pitfalls,” Clin. Neurosurg. 55, 20–26 (2008).

Front. Oncol. (1)

P. Charalampaki, M. Nakamura, D. Athanasopoulos, and A. Heimann, “Confocal-assisted multispectral fluorescent microscopy for brain tumor surgery,” Front. Oncol. 9, 583 (2019).
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Front. Surg. (2)

E. Belykh, N. L. Martirosyan, K. Yagmurlu, E. J. Miller, J. M. Eschbacher, M. Izadyyazdanabadi, L. A. Bardonova, V. A. Byvaltsev, P. Nakaji, and M. C. Preul, “Intraoperative fluorescence imaging for personalized brain tumor resection: Current state and future directions,” Front. Surg. 3, 55 (2016).
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N. Lakomkin and C. G. Hadjipanayis, “The use of spectroscopy handheld tools in brain tumor surgery: Current evidence and techniques,” Front. Surg. 6, 30 (2019).
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J. Ben Arous, J. Binding, J.-F. Leger, M. Casado, P. Topilko, L. Bourdieu, S. Gigan, and A. C. Boccara, “Single myelin fiber imaging in living rodents without labeling by deep optical coherence microscopy,” J. Biomed. Opt. 16(11), 116012 (2011).
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C. Glazowski and M. Rajadhyaksha, “Optimal detection pinhole for lowering speckle noise while maintaining adequate optical sectioning in confocal reflectance microscopes,” J. Biomed. Opt. 17(8), 085001 (2012).
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A. Alfonso-Garcia, J. Bec, S. S. Weaver, B. Hartl, J. Unger, M. Bobinski, M. Lechpammer, F. Girgis, J. Boggan, and L. Marcu, “Real-time augmented reality for delineation of surgical margins during neurosurgery using autofluorescence lifetime contrast,” J. Biophotonics 13(1), 108 (2020).
[Crossref]

J. Neuro-Oncol. (1)

F. Forest, E. Cinotti, V. Yvorel, C. Habougit, F. Vassal, C. Nuti, J.-L. Perrot, B. Labeille, and M. Péoc’h, “Ex vivo confocal microscopy imaging to identify tumor tissue on freshly removed brain sample,” J. Neuro-Oncol. 124(2), 157–164 (2015).
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J. Neuropathol. & Exp. Neurol. (1)

J. M. Eschbacher, J. F. Georges, E. Belykh, M. I. Yazdanabadi, N. L. Martirosyan, E. Szeto, C. Y. Seiler, M. A. Mooney, J. K. Daniels, K. Y. Goehring, K. R. Van Keuren-Jensen, M. C. Preul, S. W. Coons, S. Mehta, and P. Nakaji, “Immediate label-free ex vivo evaluation of human brain tumor biopsies with confocal reflectance microscopy,” J. Neuropathol. & Exp. Neurol. 76(12), 1008–1022 (2017).
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A. J. Schain, R. A. Hill, and J. Grutzendler, “Label-free in vivo imaging of myelinated axons in health and disease with spectral confocal reflectance microscopy,” Nat. Med. 20(4), 443–449 (2014).
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Nat. Methods (1)

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A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. H. van de Velde, and J. V. Frangioni, “Image-guided cancer surgery using near-infrared fluorescence,” Nat. Rev. Clin. Oncol. 10(9), 507–518 (2013).
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NeuroImage: Clin. (1)

O. Assayag, K. Grieve, B. Devaux, F. Harms, J. Pallud, F. Chretien, C. Boccara, and P. Varlet, “Imaging of non-tumorous and tumorous human brain tissues with full-field optical coherence tomography,” NeuroImage: Clin. 2, 549–557 (2013).
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D. Y. Zhang, S. Singhal, and J. Y. K. Lee, “Optical principles of fluorescence-guided brain tumor surgery: A practical primer for the neurosurgeon,” Neurosurg. 85(3), 312–324 (2019).
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T. Sankar, P. M. Delaney, R. W. Ryan, J. Eschbacher, M. Abdelwahab, P. Nakaji, S. W. Coons, A. C. Scheck, K. A. Smith, R. F. Spetzler, and M. C. Preul, “Miniaturized handheld confocal microscopy for neurosurgery results in an experimental glioblastoma model,” Neurosurg. 66(2), 410–418 (2010).
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N. L. Martirosyan, J. M. Eschbacher, M. Y. S. Kalani, J. D. Turner, E. Belykh, R. F. Spetzler, P. Nakaji, and M. C. Preul, “Prospective evaluation of the utility of intraoperative confocal laser endomicroscopy in patients with brain neoplasms using fluorescein sodium: experience with 74 cases,” Neurosurg. Focus. 40(3), E11 (2016).
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K. Erkmen, K. Bekelis, N. E. Simmons, P. A. Valdes, D. W. Roberts, K. D. Paulsen, F. Leblond, B. T. Harris, A. Kim, and B. C. Wilson, “5-aminolevulinic acid-induced protoporphyrin IX fluorescence in meningioma: Qualitative and quantitative measurements in vivo,” Oper. Neurosurg. 10(1), 74–83 (2014).
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A. Grosche, J. Grosche, M. Tackenberg, D. Scheller, G. Gerstner, A. Gumprecht, T. Pannicke, P. G. Hirrlinger, U. Wilhelmsson, and K. Hüttmann, “Versatile and simple approach to determine astrocyte territories in mouse neocortex and hippocampus,” PLoS One 8(7), e69143 (2013).
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W. Stummer, U. Pichlmeier, T. Meinel, O. D. Wiestler, F. Zanella, and H.-J. Reulen, “Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial,” The Lancet Oncol. 7(5), 392–401 (2006).
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C. Cheyuo, W. Grand, and L. L. Balos, “Near-infrared confocal laser reflectance cytoarchitectural imaging of the substantia nigra and cerebellum in the fresh human cadaver,” World Neurosurg. 97, 465–470 (2017).
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Figures (5)

Fig. 1.
Fig. 1. Microscope design and physical layout. (a) Schematic drawing of the imaging system. Components are individually labelled and full description is given in the dotted box. (b) Physical layout of microscope system taking up a 200 mm $\times$ 550 mm bench-top footprint. The inset shows a magnified view indicating the insertion of a scalpel between the microscope and sample.
Fig. 2.
Fig. 2. Zemax evaluation of system imaging performance. (a) Theoretical SR variation as a function of MEMS mirror MSAs in both x- (red) and y-directions (blue). DLP of $0.8$ SR at the objective back aperture and the system optimisation result of $0.7$ SR for all MSAs along both scan directions are indicated with horizontal lines. (b) Diffraction encircled energy versus radius from centroid in milliradians for different MSAs. Black curve is shown for DLP. Solid black line marks $86\%$ of the total energy. Magnified plot highlights radius values at which the diffraction encircled energy reach $86\%$ of the total energy for DLP and all other MSAs. (c) Huygens PSF profiles across a half FOV for both x- and y-scans. Intensity is individually normalised and displayed on a logarithmic scale. Scale bar: 200 milliradians.
Fig. 3.
Fig. 3. Imaging of 60-µm thick fixed brain slice from a Thy1-GFP mouse. (a) Top-most border of cerebral cortex showing longitudinal fissure. Yellow line: edge of sample. (b) Upper cortical region displaying densely packed dark neurons. Adjacent regions above and below featured sparser distributions of scattered cells. (c) Lower cortical region featuring the corpus callosum (CC) and neurons of varying sizes. Magenta line: outer border of the hippocampus. (d) CA1 field of the hippocampus. Pyramidal cells formed a neat hypo-reflective cell body layer (CBL). Neuronal processes (NP) were distinguished as distinct dark grooves projecting from the CA1 neurons in a parallel configuration, as well as regions with high reflective signal. Scale bar: 100 µm.
Fig. 4.
Fig. 4. Volumetric imaging of the mouse calvaria at locations where the bone surface was approximately (a-c) normal to the optical axis and (d-m) tilted by several degrees. (a) In the hard bone, the locations of osteocytes were revealed by negative contrast from the bright hard bone matrix. (b) The top surface of a bone marrow cavity was observed 45 µm below the hard bone surface. A sharp interface was visible between the hard bone and bone marrow (dotted line). (c) A further 5 µm deeper, the bone marrow cavity was larger, occupying almost the entirety of the FOV. (d-l) Consecutive slices within the calvaria showing a distinct cross-section of the hard bone matrix at each depth. Osteocytes within magenta boxes gradually come into focus from (d) to (f). (m) 3D reconstruction of (d-l) showed a smooth transition of the bone surface. The similar osteocyte pattern as in (d-f) was observed. Scale bar: 100 µm.
Fig. 5.
Fig. 5. Rotational views of maximum projected 100-µm deep organotypic hippocampal slices at $0^{\circ }$, $30^{\circ }$, and $60^{\circ }$ relative to the normal projection. (a) Schematic diagram of the rat hippocampus. Solid red boxes indicate imaging regions for (b) - (d). DG: dentate gyrus. (b) MIP of the DG showed a dark granular cell layer and adjacent regions of NPs with high reflectivity and dense fibrillarity. (c) MIP of the CA3 field showed a narrower layer of NPs surrounding a region of dark pyramidal cells. (d) Visible reflective signal contrast was also seen between the cell bodies and NPs in the CA1 field. An image from 100 µm deep in the sample is shown for each imaging region. Scale bar: 100 µm.

Tables (1)

Tables Icon

Table 1. Theoretical 1 / e 2 width and FWHM of effective IPSF for DLP and different MSAs in the proposed confocal system.