Abstract

Image-guided surgery can enhance cancer treatment by decreasing, and ideally eliminating, positive tumor margins and iatrogenic damage to healthy tissue. Current state-of-the-art near-infrared fluorescence imaging systems are bulky and costly, lack sensitivity under surgical illumination, and lack co-registration accuracy between multimodal images. As a result, an overwhelming majority of physicians still rely on their unaided eyes and palpation as the primary sensing modalities for distinguishing cancerous from healthy tissue. Here we introduce an innovative design, comprising an artificial multispectral sensor inspired by the Morpho butterfly’s compound eye, which can significantly improve image-guided surgery. By monolithically integrating spectral tapetal filters with photodetectors, we have realized a single-chip multispectral imager with 1000× higher sensitivity and 7× better spatial co-registration accuracy compared to clinical imaging systems in current use. Preclinical and clinical data demonstrate that this technology seamlessly integrates into the surgical workflow while providing surgeons with real-time information on the location of cancerous tissue and sentinel lymph nodes. Due to its low manufacturing cost, our bio-inspired sensor will provide resource-limited hospitals with much-needed technology to enable more accurate value-based health care.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

Full Article  |  PDF Article
OSA Recommended Articles
Single camera imaging system for color and near-infrared fluorescence image guided surgery

Zhenyue Chen, Nan Zhu, Shaun Pacheco, Xia Wang, and Rongguang Liang
Biomed. Opt. Express 5(8) 2791-2797 (2014)

Real-time cancer detection with an integrated lensless fluorescence contact imager

Efthymios P. Papageorgiou, Hui Zhang, Simeon Giverts, Catherine Park, Bernhard E. Boser, and Mekhail Anwar
Biomed. Opt. Express 9(8) 3607-3623 (2018)

Methods for detecting host genetic modifiers of tumor vascular function using dynamic near-infrared fluorescence imaging

Jaidip Jagtap, Gayatri Sharma, Abdul K. Parchur, Venkateswara Gogineni, Carmen Bergom, Sarah White, Michael J. Flister, and Amit Joshi
Biomed. Opt. Express 9(2) 543-556 (2018)

References

  • View by:
  • |
  • |
  • |

  1. D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
    [Crossref]
  2. S. A. McLaughlin, “Surgical management of the breast: breast conservation therapy and mastectomy,” Surg. Clin. N. Am. 93, 411–428 (2013).
    [Crossref]
  3. L. Gao and L. V. Wang, “A review of snapshot multidimensional optical imaging: measuring photon tags in parallel,” Phys. Rep. 616, 1–37 (2016).
    [Crossref]
  4. S. H. Yun and S. J. J. Kwok, “Light in diagnosis, therapy and surgery,” Nat. Biomed. Eng. 1, 0008 (2017).
    [Crossref]
  5. G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
    [Crossref]
  6. 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, 507–518 (2013).
    [Crossref]
  7. G. Hong, A. L. Antaris, and H. Dai, “Near-infrared fluorophores for biomedical imaging,” Nat. Biomed. Eng. 1, 0010 (2017).
    [Crossref]
  8. W. H. Miller and G. D. Bernard, “Butterfly glow,” J. Ultrastruct. Res. 24, 286–294 (1968).
    [Crossref]
  9. D. G. Stavenga, “Visual adaptation in butterflies,” Nature 254, 435–437 (1975).
    [Crossref]
  10. Y. Zhao, M. A. Belkin, and A. Alù, “Twisted optical metamaterials for planarized ultrathin broadband circular polarizers,” Nat. Commun. 3, 870 (2012).
    [Crossref]
  11. Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
    [Crossref]
  12. H. Liu, Y. Huang, and H. Jiang, “Artificial eye for scotopic vision with bioinspired all-optical photosensitivity enhancer,” Proc. Natl. Acad. Sci. USA 113, 3982–3985 (2016).
    [Crossref]
  13. C. Posch, T. Serrano-Gotarredona, B. Linares-Barranco, and T. Delbruck, “Retinomorphic event-based vision sensors: bioinspired cameras with spiking output,” Proc. IEEE 102, 1470–1484 (2014).
    [Crossref]
  14. T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
    [Crossref]
  15. M. Garcia, C. Edmiston, R. Marinov, A. Vail, and V. Gruev, “Bio-inspired color-polarization imager for real-time in situ imaging,” Optica 4, 1263–1271 (2017).
    [Crossref]
  16. S.-C. Liu and T. Delbruck, “Neuromorphic sensory systems,” Curr. Opin. Neurobiol. 20, 288–295 (2010).
    [Crossref]
  17. B. Wen and K. Boahen, “A silicon cochlea with active coupling,” IEEE Trans. Biomed. Circuits Syst. 3, 444–455 (2009).
    [Crossref]
  18. G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
    [Crossref]
  19. M. F. Land and D.-E. Nilsson, Animal Eyes (Oxford University, 2012).
  20. A. R. Parker, R. C. McPhedran, D. R. McKenzie, L. C. Botten, and N. Nicorovici, “Photonic engineering. Aphrodite’s iridescence,” Nature 409, 36–37 (2001).
    [Crossref]
  21. P. Vukusic and J. R. Sambles, “Photonic structures in biology,” Nature 424, 852–855 (2003).
    [Crossref]
  22. R. A. Potyrailo, H. Ghiradella, A. Vertiatchikh, K. Dovidenko, J. R. Cournoyer, and E. Olson, “Morpho butterfly wing scales demonstrate highly selective vapour response,” Nat. Photonics 1, 123–128 (2007).
    [Crossref]
  23. A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
    [Crossref]
  24. L. V. Wang and H.-I. Wu, Biomedical Optics: Principles and Imaging (Wiley, 2009).
  25. L. J. Steven, “Optical properties of biological tissues: a review,” Phys. Med. Biol. 58, R37–R61 (2013).
    [Crossref]
  26. A. V. Dsouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. 21, 080901 (2016).
    [Crossref]
  27. Z. Chen, N. Zhu, S. Pacheco, X. Wang, and R. Liang, “Single camera imaging system for color and near-infrared fluorescence image guided surgery,” Biomed. Opt. Express 5, 2791–2797 (2014).
    [Crossref]
  28. S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
    [Crossref]
  29. J. A. Hanley and B. J. McNeil, “A method of comparing the areas under receiver operating characteristic curves derived from the same cases,” Radiology 148, 839–843 (1983).
    [Crossref]
  30. M. G. Niebling, R. G. Pleijhuis, E. Bastiaannet, A. H. Brouwers, G. M. van Dam, and H. J. Hoekstra, “A systematic review and meta-analyses of sentinel lymph node identification in breast cancer and melanoma, a plea for tracer mapping,” Eur. J. Surg. Oncol. 42, 466–473 (2016).
    [Crossref]

2017 (3)

S. H. Yun and S. J. J. Kwok, “Light in diagnosis, therapy and surgery,” Nat. Biomed. Eng. 1, 0008 (2017).
[Crossref]

G. Hong, A. L. Antaris, and H. Dai, “Near-infrared fluorophores for biomedical imaging,” Nat. Biomed. Eng. 1, 0010 (2017).
[Crossref]

M. Garcia, C. Edmiston, R. Marinov, A. Vail, and V. Gruev, “Bio-inspired color-polarization imager for real-time in situ imaging,” Optica 4, 1263–1271 (2017).
[Crossref]

2016 (4)

H. Liu, Y. Huang, and H. Jiang, “Artificial eye for scotopic vision with bioinspired all-optical photosensitivity enhancer,” Proc. Natl. Acad. Sci. USA 113, 3982–3985 (2016).
[Crossref]

L. Gao and L. V. Wang, “A review of snapshot multidimensional optical imaging: measuring photon tags in parallel,” Phys. Rep. 616, 1–37 (2016).
[Crossref]

A. V. Dsouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. 21, 080901 (2016).
[Crossref]

M. G. Niebling, R. G. Pleijhuis, E. Bastiaannet, A. H. Brouwers, G. M. van Dam, and H. J. Hoekstra, “A systematic review and meta-analyses of sentinel lymph node identification in breast cancer and melanoma, a plea for tracer mapping,” Eur. J. Surg. Oncol. 42, 466–473 (2016).
[Crossref]

2015 (1)

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

2014 (4)

Z. Chen, N. Zhu, S. Pacheco, X. Wang, and R. Liang, “Single camera imaging system for color and near-infrared fluorescence image guided surgery,” Biomed. Opt. Express 5, 2791–2797 (2014).
[Crossref]

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

C. Posch, T. Serrano-Gotarredona, B. Linares-Barranco, and T. Delbruck, “Retinomorphic event-based vision sensors: bioinspired cameras with spiking output,” Proc. IEEE 102, 1470–1484 (2014).
[Crossref]

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

2013 (4)

S. A. McLaughlin, “Surgical management of the breast: breast conservation therapy and mastectomy,” Surg. Clin. N. Am. 93, 411–428 (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, 507–518 (2013).
[Crossref]

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

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

2012 (2)

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
[Crossref]

Y. Zhao, M. A. Belkin, and A. Alù, “Twisted optical metamaterials for planarized ultrathin broadband circular polarizers,” Nat. Commun. 3, 870 (2012).
[Crossref]

2011 (2)

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

2010 (1)

S.-C. Liu and T. Delbruck, “Neuromorphic sensory systems,” Curr. Opin. Neurobiol. 20, 288–295 (2010).
[Crossref]

2009 (1)

B. Wen and K. Boahen, “A silicon cochlea with active coupling,” IEEE Trans. Biomed. Circuits Syst. 3, 444–455 (2009).
[Crossref]

2007 (1)

R. A. Potyrailo, H. Ghiradella, A. Vertiatchikh, K. Dovidenko, J. R. Cournoyer, and E. Olson, “Morpho butterfly wing scales demonstrate highly selective vapour response,” Nat. Photonics 1, 123–128 (2007).
[Crossref]

2003 (1)

P. Vukusic and J. R. Sambles, “Photonic structures in biology,” Nature 424, 852–855 (2003).
[Crossref]

2001 (1)

A. R. Parker, R. C. McPhedran, D. R. McKenzie, L. C. Botten, and N. Nicorovici, “Photonic engineering. Aphrodite’s iridescence,” Nature 409, 36–37 (2001).
[Crossref]

1983 (1)

J. A. Hanley and B. J. McNeil, “A method of comparing the areas under receiver operating characteristic curves derived from the same cases,” Radiology 148, 839–843 (1983).
[Crossref]

1975 (1)

D. G. Stavenga, “Visual adaptation in butterflies,” Nature 254, 435–437 (1975).
[Crossref]

1968 (1)

W. H. Miller and G. D. Bernard, “Butterfly glow,” J. Ultrastruct. Res. 24, 286–294 (1968).
[Crossref]

Achilefu, S.

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Akers, W.

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

Alù, A.

Y. Zhao, M. A. Belkin, and A. Alù, “Twisted optical metamaterials for planarized ultrathin broadband circular polarizers,” Nat. Commun. 3, 870 (2012).
[Crossref]

Antaris, A. L.

G. Hong, A. L. Antaris, and H. Dai, “Near-infrared fluorophores for biomedical imaging,” Nat. Biomed. Eng. 1, 0010 (2017).
[Crossref]

Arthur, J.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Arts, H. J. G.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Bart, J.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Bastiaannet, E.

M. G. Niebling, R. G. Pleijhuis, E. Bastiaannet, A. H. Brouwers, G. M. van Dam, and H. J. Hoekstra, “A systematic review and meta-analyses of sentinel lymph node identification in breast cancer and melanoma, a plea for tracer mapping,” Eur. J. Surg. Oncol. 42, 466–473 (2016).
[Crossref]

Belkin, M. A.

Y. Zhao, M. A. Belkin, and A. Alù, “Twisted optical metamaterials for planarized ultrathin broadband circular polarizers,” Nat. Commun. 3, 870 (2012).
[Crossref]

Bernard, G. D.

W. H. Miller and G. D. Bernard, “Butterfly glow,” J. Ultrastruct. Res. 24, 286–294 (1968).
[Crossref]

Boahen, K.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

B. Wen and K. Boahen, “A silicon cochlea with active coupling,” IEEE Trans. Biomed. Circuits Syst. 3, 444–455 (2009).
[Crossref]

Botten, L. C.

A. R. Parker, R. C. McPhedran, D. R. McKenzie, L. C. Botten, and N. Nicorovici, “Photonic engineering. Aphrodite’s iridescence,” Nature 409, 36–37 (2001).
[Crossref]

Brouwers, A. H.

M. G. Niebling, R. G. Pleijhuis, E. Bastiaannet, A. H. Brouwers, G. M. van Dam, and H. J. Hoekstra, “A systematic review and meta-analyses of sentinel lymph node identification in breast cancer and melanoma, a plea for tracer mapping,” Eur. J. Surg. Oncol. 42, 466–473 (2016).
[Crossref]

Cauwenberghs, G.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Charanya, T.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Chen, Z.

Choi, K.-J.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Cochran, A. J.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Cournoyer, J. R.

R. A. Potyrailo, H. Ghiradella, A. Vertiatchikh, K. Dovidenko, J. R. Cournoyer, and E. Olson, “Morpho butterfly wing scales demonstrate highly selective vapour response,” Nat. Photonics 1, 123–128 (2007).
[Crossref]

Coventry, B. J.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Crane, L. M. A.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Cronin, T. W.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Crozier, K. B.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Dai, H.

G. Hong, A. L. Antaris, and H. Dai, “Near-infrared fluorophores for biomedical imaging,” Nat. Biomed. Eng. 1, 0010 (2017).
[Crossref]

de Jong, J. S.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Delbruck, T.

C. Posch, T. Serrano-Gotarredona, B. Linares-Barranco, and T. Delbruck, “Retinomorphic event-based vision sensors: bioinspired cameras with spiking output,” Proc. IEEE 102, 1470–1484 (2014).
[Crossref]

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

S.-C. Liu and T. Delbruck, “Neuromorphic sensory systems,” Curr. Opin. Neurobiol. 20, 288–295 (2010).
[Crossref]

Deng, T.

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
[Crossref]

Dovidenko, K.

R. A. Potyrailo, H. Ghiradella, A. Vertiatchikh, K. Dovidenko, J. R. Cournoyer, and E. Olson, “Morpho butterfly wing scales demonstrate highly selective vapour response,” Nat. Photonics 1, 123–128 (2007).
[Crossref]

Dsouza, A. V.

A. V. Dsouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. 21, 080901 (2016).
[Crossref]

Dudek, P.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Edmiston, C.

Elashoff, R.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Etienne-Cummings, R.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Faries, M. B.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Fields, R.

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

Folowosele, F.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Frangioni, J. V.

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, 507–518 (2013).
[Crossref]

Gao, L.

L. Gao and L. V. Wang, “A review of snapshot multidimensional optical imaging: measuring photon tags in parallel,” Phys. Rep. 616, 1–37 (2016).
[Crossref]

Gao, S.

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Garcia, M.

Ghiradella, H.

R. A. Potyrailo, H. Ghiradella, A. Vertiatchikh, K. Dovidenko, J. R. Cournoyer, and E. Olson, “Morpho butterfly wing scales demonstrate highly selective vapour response,” Nat. Photonics 1, 123–128 (2007).
[Crossref]

Ghiradella, H. T.

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
[Crossref]

Gruev, V.

M. Garcia, C. Edmiston, R. Marinov, A. Vail, and V. Gruev, “Bio-inspired color-polarization imager for real-time in situ imaging,” Optica 4, 1263–1271 (2017).
[Crossref]

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Häfliger, P.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Hamilton, T.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Hanley, J. A.

J. A. Hanley and B. J. McNeil, “A method of comparing the areas under receiver operating characteristic curves derived from the same cases,” Radiology 148, 839–843 (1983).
[Crossref]

Harlaar, N. J.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Henderson, E. R.

A. V. Dsouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. 21, 080901 (2016).
[Crossref]

Hoekstra, H. J.

M. G. Niebling, R. G. Pleijhuis, E. Bastiaannet, A. H. Brouwers, G. M. van Dam, and H. J. Hoekstra, “A systematic review and meta-analyses of sentinel lymph node identification in breast cancer and melanoma, a plea for tracer mapping,” Eur. J. Surg. Oncol. 42, 466–473 (2016).
[Crossref]

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Hong, G.

G. Hong, A. L. Antaris, and H. Dai, “Near-infrared fluorophores for biomedical imaging,” Nat. Biomed. Eng. 1, 0010 (2017).
[Crossref]

Huang, Y.

H. Liu, Y. Huang, and H. Jiang, “Artificial eye for scotopic vision with bioinspired all-optical photosensitivity enhancer,” Proc. Natl. Acad. Sci. USA 113, 3982–3985 (2016).
[Crossref]

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Hutteman, M.

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, 507–518 (2013).
[Crossref]

Hynna, K.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Indiveri, G.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Jiang, H.

H. Liu, Y. Huang, and H. Jiang, “Artificial eye for scotopic vision with bioinspired all-optical photosensitivity enhancer,” Proc. Natl. Acad. Sci. USA 113, 3982–3985 (2016).
[Crossref]

Jung, I.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Kahan, L.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Karakousis, C. P.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Kashani-Sabet, M.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Kelder, W.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Kim, R.-H.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Kraybill, W. G.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Kwok, S. J. J.

S. H. Yun and S. J. J. Kwok, “Light in diagnosis, therapy and surgery,” Nat. Biomed. Eng. 1, 0008 (2017).
[Crossref]

Lake, S. P.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Land, M. F.

M. F. Land and D.-E. Nilsson, Animal Eyes (Oxford University, 2012).

Li, R.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Liang, R.

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

Z. Chen, N. Zhu, S. Pacheco, X. Wang, and R. Liang, “Single camera imaging system for color and near-infrared fluorescence image guided surgery,” Biomed. Opt. Express 5, 2791–2797 (2014).
[Crossref]

Lin, H.

A. V. Dsouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. 21, 080901 (2016).
[Crossref]

Linares-Barranco, B.

C. Posch, T. Serrano-Gotarredona, B. Linares-Barranco, and T. Delbruck, “Retinomorphic event-based vision sensors: bioinspired cameras with spiking output,” Proc. IEEE 102, 1470–1484 (2014).
[Crossref]

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Liu, H.

H. Liu, Y. Huang, and H. Jiang, “Artificial eye for scotopic vision with bioinspired all-optical photosensitivity enhancer,” Proc. Natl. Acad. Sci. USA 113, 3982–3985 (2016).
[Crossref]

Liu, S.-C.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

S.-C. Liu and T. Delbruck, “Neuromorphic sensory systems,” Curr. Opin. Neurobiol. 20, 288–295 (2010).
[Crossref]

Liu, Z.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Low, P. S.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Lu, C.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Malyarchuk, V.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Margenthaler, J.

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

Marinov, R.

Marshall, J.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

McKenzie, D. R.

A. R. Parker, R. C. McPhedran, D. R. McKenzie, L. C. Botten, and N. Nicorovici, “Photonic engineering. Aphrodite’s iridescence,” Nature 409, 36–37 (2001).
[Crossref]

McKinnon, J. G.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

McLaughlin, S. A.

S. A. McLaughlin, “Surgical management of the breast: breast conservation therapy and mastectomy,” Surg. Clin. N. Am. 93, 411–428 (2013).
[Crossref]

McNeil, B. J.

J. A. Hanley and B. J. McNeil, “A method of comparing the areas under receiver operating characteristic curves derived from the same cases,” Radiology 148, 839–843 (1983).
[Crossref]

McPhedran, R. C.

A. R. Parker, R. C. McPhedran, D. R. McKenzie, L. C. Botten, and N. Nicorovici, “Photonic engineering. Aphrodite’s iridescence,” Nature 409, 36–37 (2001).
[Crossref]

Miller, W. H.

W. H. Miller and G. D. Bernard, “Butterfly glow,” J. Ultrastruct. Res. 24, 286–294 (1968).
[Crossref]

Mondal, S.

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

Morris, W. G.

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
[Crossref]

Morton, D. L.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Mozzillo, N.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Nicorovici, N.

A. R. Parker, R. C. McPhedran, D. R. McKenzie, L. C. Botten, and N. Nicorovici, “Photonic engineering. Aphrodite’s iridescence,” Nature 409, 36–37 (2001).
[Crossref]

Niebling, M. G.

M. G. Niebling, R. G. Pleijhuis, E. Bastiaannet, A. H. Brouwers, G. M. van Dam, and H. J. Hoekstra, “A systematic review and meta-analyses of sentinel lymph node identification in breast cancer and melanoma, a plea for tracer mapping,” Eur. J. Surg. Oncol. 42, 466–473 (2016).
[Crossref]

Nieweg, O. E.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Nilsson, D.-E.

M. F. Land and D.-E. Nilsson, Animal Eyes (Oxford University, 2012).

Ntziachristos, V.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Olson, E.

R. A. Potyrailo, H. Ghiradella, A. Vertiatchikh, K. Dovidenko, J. R. Cournoyer, and E. Olson, “Morpho butterfly wing scales demonstrate highly selective vapour response,” Nat. Photonics 1, 123–128 (2007).
[Crossref]

Pacheco, S.

Park, H.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Parker, A. R.

A. R. Parker, R. C. McPhedran, D. R. McKenzie, L. C. Botten, and N. Nicorovici, “Photonic engineering. Aphrodite’s iridescence,” Nature 409, 36–37 (2001).
[Crossref]

Paul, E.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Pleijhuis, R. G.

M. G. Niebling, R. G. Pleijhuis, E. Bastiaannet, A. H. Brouwers, G. M. van Dam, and H. J. Hoekstra, “A systematic review and meta-analyses of sentinel lymph node identification in breast cancer and melanoma, a plea for tracer mapping,” Eur. J. Surg. Oncol. 42, 466–473 (2016).
[Crossref]

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Pogue, B. W.

A. V. Dsouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. 21, 080901 (2016).
[Crossref]

Posch, C.

C. Posch, T. Serrano-Gotarredona, B. Linares-Barranco, and T. Delbruck, “Retinomorphic event-based vision sensors: bioinspired cameras with spiking output,” Proc. IEEE 102, 1470–1484 (2014).
[Crossref]

Potyrailo, R. A.

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
[Crossref]

R. A. Potyrailo, H. Ghiradella, A. Vertiatchikh, K. Dovidenko, J. R. Cournoyer, and E. Olson, “Morpho butterfly wing scales demonstrate highly selective vapour response,” Nat. Photonics 1, 123–128 (2007).
[Crossref]

Powell, S. B.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Pris, A. D.

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
[Crossref]

Puleo, C. A.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Raman, B.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Renaud, S.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Roberts, N. W.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Rogers, J. A.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Roses, D. F.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Saha, D.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Saïghi, S.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Sambles, J. R.

P. Vukusic and J. R. Sambles, “Photonic structures in biology,” Nature 424, 852–855 (2003).
[Crossref]

Samkoe, K. S.

A. V. Dsouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. 21, 080901 (2016).
[Crossref]

Sarantopoulos, A.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Schemmel, J.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Serrano-Gotarredona, T.

C. Posch, T. Serrano-Gotarredona, B. Linares-Barranco, and T. Delbruck, “Retinomorphic event-based vision sensors: bioinspired cameras with spiking output,” Proc. IEEE 102, 1470–1484 (2014).
[Crossref]

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Smithers, B. M.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Som, A.

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

Song, Y. M.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Stavenga, D. G.

D. G. Stavenga, “Visual adaptation in butterflies,” Nature 254, 435–437 (1975).
[Crossref]

Steven, L. J.

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

Sudlow, G.

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

Surman, C.

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
[Crossref]

Themelis, G.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Thompson, J. F.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Utturkar, Y.

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (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, 507–518 (2013).
[Crossref]

Vail, A.

van Dam, G. M.

M. G. Niebling, R. G. Pleijhuis, E. Bastiaannet, A. H. Brouwers, G. M. van Dam, and H. J. Hoekstra, “A systematic review and meta-analyses of sentinel lymph node identification in breast cancer and melanoma, a plea for tracer mapping,” Eur. J. Surg. Oncol. 42, 466–473 (2016).
[Crossref]

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[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, 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, 507–518 (2013).
[Crossref]

van der Zee, A. G. J.

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

van Schaik, A.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Vert, A.

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
[Crossref]

Vertiatchikh, A.

R. A. Potyrailo, H. Ghiradella, A. Vertiatchikh, K. Dovidenko, J. R. Cournoyer, and E. Olson, “Morpho butterfly wing scales demonstrate highly selective vapour response,” Nat. Photonics 1, 123–128 (2007).
[Crossref]

Vukusic, P.

P. Vukusic and J. R. Sambles, “Photonic structures in biology,” Nature 424, 852–855 (2003).
[Crossref]

Wang, H.-J.

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Wang, L. V.

L. Gao and L. V. Wang, “A review of snapshot multidimensional optical imaging: measuring photon tags in parallel,” Phys. Rep. 616, 1–37 (2016).
[Crossref]

L. V. Wang and H.-I. Wu, Biomedical Optics: Principles and Imaging (Wiley, 2009).

Wang, X.

Wang, Y.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Wen, B.

B. Wen and K. Boahen, “A silicon cochlea with active coupling,” IEEE Trans. Biomed. Circuits Syst. 3, 444–455 (2009).
[Crossref]

Wijekoon, J.

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

Wu, H.-I.

L. V. Wang and H.-I. Wu, Biomedical Optics: Principles and Imaging (Wiley, 2009).

Xiao, J.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

Xie, Y.

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

York, T.

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Yun, S. H.

S. H. Yun and S. J. J. Kwok, “Light in diagnosis, therapy and surgery,” Nat. Biomed. Eng. 1, 0008 (2017).
[Crossref]

Zalyubovskiy, S.

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
[Crossref]

Zhao, Y.

Y. Zhao, M. A. Belkin, and A. Alù, “Twisted optical metamaterials for planarized ultrathin broadband circular polarizers,” Nat. Commun. 3, 870 (2012).
[Crossref]

Zhu, N.

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

Z. Chen, N. Zhu, S. Pacheco, X. Wang, and R. Liang, “Single camera imaging system for color and near-infrared fluorescence image guided surgery,” Biomed. Opt. Express 5, 2791–2797 (2014).
[Crossref]

Biomed. Opt. Express (1)

Curr. Opin. Neurobiol. (1)

S.-C. Liu and T. Delbruck, “Neuromorphic sensory systems,” Curr. Opin. Neurobiol. 20, 288–295 (2010).
[Crossref]

Eur. J. Surg. Oncol. (1)

M. G. Niebling, R. G. Pleijhuis, E. Bastiaannet, A. H. Brouwers, G. M. van Dam, and H. J. Hoekstra, “A systematic review and meta-analyses of sentinel lymph node identification in breast cancer and melanoma, a plea for tracer mapping,” Eur. J. Surg. Oncol. 42, 466–473 (2016).
[Crossref]

Front. Neurosci. (1)

G. Indiveri, B. Linares-Barranco, T. Hamilton, A. van Schaik, R. Etienne-Cummings, T. Delbruck, S.-C. Liu, P. Dudek, P. Häfliger, S. Renaud, J. Schemmel, G. Cauwenberghs, J. Arthur, K. Hynna, F. Folowosele, S. Saïghi, T. Serrano-Gotarredona, J. Wijekoon, Y. Wang, and K. Boahen, “Neuromorphic silicon neuron circuits,” Front. Neurosci. 5, 73 (2011).
[Crossref]

IEEE Trans. Biomed. Circuits Syst. (1)

B. Wen and K. Boahen, “A silicon cochlea with active coupling,” IEEE Trans. Biomed. Circuits Syst. 3, 444–455 (2009).
[Crossref]

J. Biomed. Opt. (1)

A. V. Dsouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery systems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. 21, 080901 (2016).
[Crossref]

J. Ultrastruct. Res. (1)

W. H. Miller and G. D. Bernard, “Butterfly glow,” J. Ultrastruct. Res. 24, 286–294 (1968).
[Crossref]

N. Engl. J. Med. (1)

D. L. Morton, J. F. Thompson, A. J. Cochran, N. Mozzillo, O. E. Nieweg, D. F. Roses, H. J. Hoekstra, C. P. Karakousis, C. A. Puleo, B. J. Coventry, M. Kashani-Sabet, B. M. Smithers, E. Paul, W. G. Kraybill, J. G. McKinnon, H.-J. Wang, R. Elashoff, and M. B. Faries, “Final trial report of sentinel-node biopsy versus nodal observation in melanoma,” N. Engl. J. Med. 370, 599–609 (2014).
[Crossref]

Nat. Biomed. Eng. (2)

S. H. Yun and S. J. J. Kwok, “Light in diagnosis, therapy and surgery,” Nat. Biomed. Eng. 1, 0008 (2017).
[Crossref]

G. Hong, A. L. Antaris, and H. Dai, “Near-infrared fluorophores for biomedical imaging,” Nat. Biomed. Eng. 1, 0010 (2017).
[Crossref]

Nat. Commun. (1)

Y. Zhao, M. A. Belkin, and A. Alù, “Twisted optical metamaterials for planarized ultrathin broadband circular polarizers,” Nat. Commun. 3, 870 (2012).
[Crossref]

Nat. Med. (1)

G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-[alpha] targeting: first in-human results,” Nat. Med. 17, 1315–1319 (2011).
[Crossref]

Nat. Photonics (2)

R. A. Potyrailo, H. Ghiradella, A. Vertiatchikh, K. Dovidenko, J. R. Cournoyer, and E. Olson, “Morpho butterfly wing scales demonstrate highly selective vapour response,” Nat. Photonics 1, 123–128 (2007).
[Crossref]

A. D. Pris, Y. Utturkar, C. Surman, W. G. Morris, A. Vert, S. Zalyubovskiy, T. Deng, H. T. Ghiradella, and R. A. Potyrailo, “Towards high-speed imaging of infrared photons with bio-inspired nanoarchitectures,” Nat. Photonics 6, 195–200 (2012).
[Crossref]

Nat. Rev. Clin. Oncol. (1)

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, 507–518 (2013).
[Crossref]

Nature (4)

D. G. Stavenga, “Visual adaptation in butterflies,” Nature 254, 435–437 (1975).
[Crossref]

Y. M. Song, Y. Xie, V. Malyarchuk, J. Xiao, I. Jung, K.-J. Choi, Z. Liu, H. Park, C. Lu, R.-H. Kim, R. Li, K. B. Crozier, Y. Huang, and J. A. Rogers, “Digital cameras with designs inspired by the arthropod eye,” Nature 497, 95–99 (2013).
[Crossref]

A. R. Parker, R. C. McPhedran, D. R. McKenzie, L. C. Botten, and N. Nicorovici, “Photonic engineering. Aphrodite’s iridescence,” Nature 409, 36–37 (2001).
[Crossref]

P. Vukusic and J. R. Sambles, “Photonic structures in biology,” Nature 424, 852–855 (2003).
[Crossref]

Optica (1)

Phys. Med. Biol. (1)

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

Phys. Rep. (1)

L. Gao and L. V. Wang, “A review of snapshot multidimensional optical imaging: measuring photon tags in parallel,” Phys. Rep. 616, 1–37 (2016).
[Crossref]

Proc. IEEE (2)

C. Posch, T. Serrano-Gotarredona, B. Linares-Barranco, and T. Delbruck, “Retinomorphic event-based vision sensors: bioinspired cameras with spiking output,” Proc. IEEE 102, 1470–1484 (2014).
[Crossref]

T. York, S. B. Powell, S. Gao, L. Kahan, T. Charanya, D. Saha, N. W. Roberts, T. W. Cronin, J. Marshall, S. Achilefu, S. P. Lake, B. Raman, and V. Gruev, “Bioinspired polarization imaging sensors: from circuits and optics to signal processing algorithms and biomedical applications,” Proc. IEEE 102, 1450–1469 (2014).
[Crossref]

Proc. Natl. Acad. Sci. USA (1)

H. Liu, Y. Huang, and H. Jiang, “Artificial eye for scotopic vision with bioinspired all-optical photosensitivity enhancer,” Proc. Natl. Acad. Sci. USA 113, 3982–3985 (2016).
[Crossref]

Radiology (1)

J. A. Hanley and B. J. McNeil, “A method of comparing the areas under receiver operating characteristic curves derived from the same cases,” Radiology 148, 839–843 (1983).
[Crossref]

Sci. Rep. (1)

S. Mondal, S. Gao, N. Zhu, G. Sudlow, A. Som, W. Akers, R. Fields, J. Margenthaler, R. Liang, V. Gruev, and S. Achilefu, “Binocular goggle augmented imaging and navigation system provides real-time fluorescence image guidance for tumor resection and sentinel lymph node mapping,” Sci. Rep. 5, 12117 (2015).
[Crossref]

Surg. Clin. N. Am. (1)

S. A. McLaughlin, “Surgical management of the breast: breast conservation therapy and mastectomy,” Surg. Clin. N. Am. 93, 411–428 (2013).
[Crossref]

Other (2)

M. F. Land and D.-E. Nilsson, Animal Eyes (Oxford University, 2012).

L. V. Wang and H.-I. Wu, Biomedical Optics: Principles and Imaging (Wiley, 2009).

Supplementary Material (4)

NameDescription
» Supplement 1       Supplemental document
» Visualization 1       Real-time image guided surgery in PyMT mouse model with multifocal tumors throughout the mammary tissues. The surgery is conducted under surgical light illumination of 60kLux and 780 nm laser light excitation with optical power of 20mW/cm2.
» Visualization 2       NIRF-color real-time imaging of tumors in PyMT mouse model after the skin has been resected and all tumors are visible. Surgery is conducted under surgical light illumination of 60kLux and 780 nm laser light excitation with optical power of 20mW/cm2
» Visualization 3       Sentinel lymph node mapping in a patient with breast cancer. Left, color image; middle, NIRF image; right, composite image captured by our bio-inspired sensor.

Cited By

OSA participates in Crossref's Cited-By Linking service. Citing articles from OSA journals and other participating publishers are listed here.

Alert me when this article is cited.


Figures (7)

Fig. 1.
Fig. 1. Our bio-inspired imaging sensor uses a new design paradigm to capture color and near-infrared fluorescence information. (a) Morpho butterfly (Morpho peleides) blue color is due to tree-shaped photonic crystals in its wings. Similar photonic crystals can be found in the butterfly’s ommatidia. (b) Close-up of the Morpho ommatidia indicating “eye-shine” due to tapetal filters together with screening and visual pigments in the rhabdom, which enable multispectral target detection. (c) Our compact bio-inspired multispectral imaging sensor combines an array of imaging elements with pixelated tapetal spectral filters. (d) Transmission electron microscope image of an individual Morpho ommatidium, which monolithically integrates tapetal filters with light-sensitive rhabdom. (e) Cross-sectional scanning electron microscope image of our bio-inspired imaging sensor. Tapetal filters combined with silicon photodetectors allow for high co-registration accuracy in the detected spectral information. Scale bar, 2 μm.
Fig. 2.
Fig. 2. (a) Measured optical density and (b) transmittance of the four tapetal spectral filters in our bio-inspired multispectral imaging sensor. (c) Spatial uniformity or fixed pattern noise (FPN) before calibration as a function of light intensity. (d) The calibrated FPN shows that the bio-inspired camera captures data with 0.1% spatial variations for uniform intensity targets. (e) Quantum efficiency of our bio-inspired image sensor. (f) Fluorescence detection limits under surgical light illumination for our bio-inspired sensor, which utilizes a multi-exposure method (green) compared with single-exposure method (blue) used in state-of-the-art pixelated color-NIR sensors. The dashed vertical lines are the individual detection thresholds for both sensors estimated as the mean value plus three standard deviations of the control vial. The bio-inspired sensor’s 1000× improvement in detection limit is achieved due to multi-exposure (P<0.0001), high NIR optical density, and high NIR quantum efficiency. Data are presented as mean±SD.
Fig. 3.
Fig. 3. Single-exposure cameras have limited capabilities for simultaneous imaging of color and near-infrared (NIR) images with high contrast under surgical light illumination. (a) Exposure time of 0.1 ms produces good color but poor NIR contrast images. (b) Exposure time of 40 ms produces oversaturated color image but good NIR contrast image. (c) Our bio-inspired camera captures color data with 0.1 ms exposure time and NIR data with 40 ms exposure time. This multi-exposure feature enables high-contrast images from both imaging modalities.
Fig. 4.
Fig. 4. Co-registration accuracy as a function of temperature: comparison between a beam-splitter NIRF system and our bio-inspired sensor at the (a) sensor plane and (b) imaging plane. Because of the monolithic integration of spectral filters with complementary metal-oxide semiconductor (CMOS) imaging elements, the co-registration between color and NIR images in our bio-inspired imaging system is independent of temperature.
Fig. 5.
Fig. 5. Color near-infrared (NIR) composite images recorded with a beam-splitter NIRF system while the instrument is at an operating temperature of (a) 15°C and (b) 32°C. The tumor-targeted probe LS301 is used to highlight the location of the tumor, which is under the sciatic nerve. The instrument is calibrated at 15°C, so the NIR and color images in (a) are correctly co-registered, and the location of the sciatic nerve is visible due to absence of fluorescence signal (arrow). In contrast, at 32°C (b), the NIR fluorescence image is spatially shifted and superimposed on the incorrect anatomic features (arrow) due to the thermal shift of individual optical elements comprising the instrument. Thus, the location of the sciatic nerve is incorrectly highlighted as cancerous tissue.
Fig. 6.
Fig. 6. (a)–(c) Snapshot images obtained with our bio-inspired imaging sensor during surgery with a spontaneous breast cancer murine model. (a) Near-infrared (NIR) image highlights the locations of the tumors as well as the liver, where the tumor-targeted contrast agent LS301 is cleared. (b) Color image of the animal obtained by our bio-inspired sensor during tumor removal. (c) Combined image of both NIR and color information as it is presented to the surgeon to assist with tumor resection. (d) Combined image of both NIR and color information indicating the location of the tumors under the skin. (See Visualization 1 and Visualization 2.)
Fig. 7.
Fig. 7. Clinical use of our bio-inspired imaging sensor for mapping sentinel lymph nodes (SLNs) using indocyanine green (ICG) contrast agent. (a) Fluorescence image obtained with the bio-inspired camera highlights the location of the SLNs. (b) Color image obtained with the sensor captures anatomical features during the surgical procedure. (c) Synthetic image obtained by combining color and near-infrared images and presented to the surgeon in the operating room to assist in determining the location of the SLNs (see Visualization 3).

Tables (3)

Tables Icon

Table 1. Optical Performance of Various State-of-the-Art Near-Infrared Fluorescence (NIRF) Imaging Systems and Our Bio-Inspired NIRF Imager

Tables Icon

Table 2. Summary of the Optoelectronic Performance of Our Bio-Inspired Imaging Sensor

Tables Icon

Table 3. Optical Performance Comparison Between Pixelated NIRF Imaging Systems and Our Bio-Inspired NIRF Imager

Metrics