Abstract

Fluorescence guided surgery has the potential to positively impact surgical oncology; current operating microscopes and stand-alone imaging systems are too insensitive or too cumbersome to maximally take advantage of new tumor-specific agents developed through the microdose pathway. To this end, a custom-built illumination and imaging module enabling picomolar-sensitive near-infrared fluorescence imaging on a commercial operating microscope is described. The limits of detection and system specifications are characterized, and in vivo efficacy of the system in detecting ABY-029 is evaluated in a rat orthotopic glioma model following microdose injections, showing the suitability of the device for microdose phase 0 clinical trials.

© 2016 Optical Society of America

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  1. A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. 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] [PubMed]
  2. Q. T. Nguyen and R. Y. Tsien, “Fluorescence-guided surgery with live molecular navigation--a new cutting edge,” Nat. Rev. Cancer 13(9), 653–662 (2013).
    [Crossref] [PubMed]
  3. B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
    [Crossref] [PubMed]
  4. G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
    [Crossref] [PubMed]
  5. 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,” Lancet Oncol. 7(5), 392–401 (2006).
    [Crossref] [PubMed]
  6. E. L. Rosenthal, B. D. Kulbersh, T. King, T. R. Chaudhuri, and K. R. Zinn, “Use of fluorescent labeled anti-epidermal growth factor receptor antibody to image head and neck squamous cell carcinoma xenografts,” Mol. Cancer Ther. 6(4), 1230–1238 (2007).
    [Crossref] [PubMed]
  7. A. V. Dsouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery sytems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. (2016, Accepted July 19).
  8. J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.
  9. Food and Drug Administration, “Guidance for Industry, Investigators, and Reviewers: Exploratory IND Studies,” Office of Training and Communication HFD-240 (2006).
  10. J. T. Elliott, A. V. Dsouza, S. C. Davis, J. D. Olson, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Review of fluorescence guided surgery visualization and overlay techniques,” Biomed. Opt. Express 6(10), 3765–3782 (2015).
    [Crossref] [PubMed]
  11. T. Kuroiwa, Y. Kajimoto, and T. Ohta, “Development of a fluorescein operative microscope for use during malignant glioma surgery: a technical note and preliminary report,” Surg. Neurol. 50(1), 41–49 (1998).
    [Crossref] [PubMed]
  12. P. A. Valdés, F. Leblond, V. L. Jacobs, B. C. Wilson, K. D. Paulsen, and D. W. Roberts, “Quantitative, spectrally-resolved intraoperative fluorescence imaging,” Sci. Rep. 2, 798 (2012).
    [Crossref] [PubMed]
  13. J. R. Watson, C. F. Gainer, N. Martirosyan, J. Skoch, G. M. Lemole, R. Anton, and M. Romanowski, “Augmented microscopy: real-time overlay of bright-field and near-infrared fluorescence images,” J. Biomed. Opt. 20(10), 106002 (2015).
    [Crossref] [PubMed]
  14. D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
    [Crossref] [PubMed]

2015 (2)

J. R. Watson, C. F. Gainer, N. Martirosyan, J. Skoch, G. M. Lemole, R. Anton, and M. Romanowski, “Augmented microscopy: real-time overlay of bright-field and near-infrared fluorescence images,” J. Biomed. Opt. 20(10), 106002 (2015).
[Crossref] [PubMed]

J. T. Elliott, A. V. Dsouza, S. C. Davis, J. D. Olson, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Review of fluorescence guided surgery visualization and overlay techniques,” Biomed. Opt. Express 6(10), 3765–3782 (2015).
[Crossref] [PubMed]

2013 (2)

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. 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] [PubMed]

Q. T. Nguyen and R. Y. Tsien, “Fluorescence-guided surgery with live molecular navigation--a new cutting edge,” Nat. Rev. Cancer 13(9), 653–662 (2013).
[Crossref] [PubMed]

2012 (1)

P. A. Valdés, F. Leblond, V. L. Jacobs, B. C. Wilson, K. D. Paulsen, and D. W. Roberts, “Quantitative, spectrally-resolved intraoperative fluorescence imaging,” Sci. Rep. 2, 798 (2012).
[Crossref] [PubMed]

2011 (2)

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

2007 (1)

E. L. Rosenthal, B. D. Kulbersh, T. King, T. R. Chaudhuri, and K. R. Zinn, “Use of fluorescent labeled anti-epidermal growth factor receptor antibody to image head and neck squamous cell carcinoma xenografts,” Mol. Cancer Ther. 6(4), 1230–1238 (2007).
[Crossref] [PubMed]

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,” Lancet Oncol. 7(5), 392–401 (2006).
[Crossref] [PubMed]

2005 (1)

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

1998 (1)

T. Kuroiwa, Y. Kajimoto, and T. Ohta, “Development of a fluorescein operative microscope for use during malignant glioma surgery: a technical note and preliminary report,” Surg. Neurol. 50(1), 41–49 (1998).
[Crossref] [PubMed]

Anton, R.

J. R. Watson, C. F. Gainer, N. Martirosyan, J. Skoch, G. M. Lemole, R. Anton, and M. Romanowski, “Augmented microscopy: real-time overlay of bright-field and near-infrared fluorescence images,” J. Biomed. Opt. 20(10), 106002 (2015).
[Crossref] [PubMed]

Arts, H. J.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Bart, J.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Berens, M. E.

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

Berens, T. J.

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

Chaudhuri, T. R.

E. L. Rosenthal, B. D. Kulbersh, T. King, T. R. Chaudhuri, and K. R. Zinn, “Use of fluorescent labeled anti-epidermal growth factor receptor antibody to image head and neck squamous cell carcinoma xenografts,” Mol. Cancer Ther. 6(4), 1230–1238 (2007).
[Crossref] [PubMed]

Coons, S. W.

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

Crane, L. M.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Davis, S. C.

J. T. Elliott, A. V. Dsouza, S. C. Davis, J. D. Olson, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Review of fluorescence guided surgery visualization and overlay techniques,” Biomed. Opt. Express 6(10), 3765–3782 (2015).
[Crossref] [PubMed]

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

de Jong, J. S.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Dsouza, A. V.

Elliott, J. T.

J. T. Elliott, A. V. Dsouza, S. C. Davis, J. D. Olson, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Review of fluorescence guided surgery visualization and overlay techniques,” Biomed. Opt. Express 6(10), 3765–3782 (2015).
[Crossref] [PubMed]

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

Evans, L. T.

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

Feldwisch, J.

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

Frangioni, J. V.

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. 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] [PubMed]

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

Gainer, C. F.

J. R. Watson, C. F. Gainer, N. Martirosyan, J. Skoch, G. M. Lemole, R. Anton, and M. Romanowski, “Augmented microscopy: real-time overlay of bright-field and near-infrared fluorescence images,” J. Biomed. Opt. 20(10), 106002 (2015).
[Crossref] [PubMed]

Harlaar, N. J.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Hoelzinger, D. B.

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

Hutteman, M.

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. 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] [PubMed]

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

Jacobs, V. L.

P. A. Valdés, F. Leblond, V. L. Jacobs, B. C. Wilson, K. D. Paulsen, and D. W. Roberts, “Quantitative, spectrally-resolved intraoperative fluorescence imaging,” Sci. Rep. 2, 798 (2012).
[Crossref] [PubMed]

Kajimoto, Y.

T. Kuroiwa, Y. Kajimoto, and T. Ohta, “Development of a fluorescein operative microscope for use during malignant glioma surgery: a technical note and preliminary report,” Surg. Neurol. 50(1), 41–49 (1998).
[Crossref] [PubMed]

Kelder, W.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

King, T.

E. L. Rosenthal, B. D. Kulbersh, T. King, T. R. Chaudhuri, and K. R. Zinn, “Use of fluorescent labeled anti-epidermal growth factor receptor antibody to image head and neck squamous cell carcinoma xenografts,” Mol. Cancer Ther. 6(4), 1230–1238 (2007).
[Crossref] [PubMed]

Kulbersh, B. D.

E. L. Rosenthal, B. D. Kulbersh, T. King, T. R. Chaudhuri, and K. R. Zinn, “Use of fluorescent labeled anti-epidermal growth factor receptor antibody to image head and neck squamous cell carcinoma xenografts,” Mol. Cancer Ther. 6(4), 1230–1238 (2007).
[Crossref] [PubMed]

Kuppen, P. J.

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

Kuroiwa, T.

T. Kuroiwa, Y. Kajimoto, and T. Ohta, “Development of a fluorescein operative microscope for use during malignant glioma surgery: a technical note and preliminary report,” Surg. Neurol. 50(1), 41–49 (1998).
[Crossref] [PubMed]

Leblond, F.

P. A. Valdés, F. Leblond, V. L. Jacobs, B. C. Wilson, K. D. Paulsen, and D. W. Roberts, “Quantitative, spectrally-resolved intraoperative fluorescence imaging,” Sci. Rep. 2, 798 (2012).
[Crossref] [PubMed]

Lemole, G. M.

J. R. Watson, C. F. Gainer, N. Martirosyan, J. Skoch, G. M. Lemole, R. Anton, and M. Romanowski, “Augmented microscopy: real-time overlay of bright-field and near-infrared fluorescence images,” J. Biomed. Opt. 20(10), 106002 (2015).
[Crossref] [PubMed]

Low, P. S.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Löwik, C. W.

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

Mariani, L.

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

Marra, K.

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

Martirosyan, N.

J. R. Watson, C. F. Gainer, N. Martirosyan, J. Skoch, G. M. Lemole, R. Anton, and M. Romanowski, “Augmented microscopy: real-time overlay of bright-field and near-infrared fluorescence images,” J. Biomed. Opt. 20(10), 106002 (2015).
[Crossref] [PubMed]

McDonough, W. S.

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

Meinel, T.

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,” Lancet Oncol. 7(5), 392–401 (2006).
[Crossref] [PubMed]

Mieog, J. S.

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

Nguyen, Q. T.

Q. T. Nguyen and R. Y. Tsien, “Fluorescence-guided surgery with live molecular navigation--a new cutting edge,” Nat. Rev. Cancer 13(9), 653–662 (2013).
[Crossref] [PubMed]

Ntziachristos, V.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Ohta, T.

T. Kuroiwa, Y. Kajimoto, and T. Ohta, “Development of a fluorescein operative microscope for use during malignant glioma surgery: a technical note and preliminary report,” Surg. Neurol. 50(1), 41–49 (1998).
[Crossref] [PubMed]

Olson, J. D.

J. T. Elliott, A. V. Dsouza, S. C. Davis, J. D. Olson, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Review of fluorescence guided surgery visualization and overlay techniques,” Biomed. Opt. Express 6(10), 3765–3782 (2015).
[Crossref] [PubMed]

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

Paulsen, K. D.

J. T. Elliott, A. V. Dsouza, S. C. Davis, J. D. Olson, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Review of fluorescence guided surgery visualization and overlay techniques,” Biomed. Opt. Express 6(10), 3765–3782 (2015).
[Crossref] [PubMed]

P. A. Valdés, F. Leblond, V. L. Jacobs, B. C. Wilson, K. D. Paulsen, and D. W. Roberts, “Quantitative, spectrally-resolved intraoperative fluorescence imaging,” Sci. Rep. 2, 798 (2012).
[Crossref] [PubMed]

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

Pichlmeier, U.

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,” Lancet Oncol. 7(5), 392–401 (2006).
[Crossref] [PubMed]

Pleijhuis, R. G.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Pogue, B. W.

J. T. Elliott, A. V. Dsouza, S. C. Davis, J. D. Olson, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Review of fluorescence guided surgery visualization and overlay techniques,” Biomed. Opt. Express 6(10), 3765–3782 (2015).
[Crossref] [PubMed]

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

Reulen, H. J.

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,” Lancet Oncol. 7(5), 392–401 (2006).
[Crossref] [PubMed]

Roberts, D. W.

J. T. Elliott, A. V. Dsouza, S. C. Davis, J. D. Olson, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Review of fluorescence guided surgery visualization and overlay techniques,” Biomed. Opt. Express 6(10), 3765–3782 (2015).
[Crossref] [PubMed]

P. A. Valdés, F. Leblond, V. L. Jacobs, B. C. Wilson, K. D. Paulsen, and D. W. Roberts, “Quantitative, spectrally-resolved intraoperative fluorescence imaging,” Sci. Rep. 2, 798 (2012).
[Crossref] [PubMed]

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

Romanowski, M.

J. R. Watson, C. F. Gainer, N. Martirosyan, J. Skoch, G. M. Lemole, R. Anton, and M. Romanowski, “Augmented microscopy: real-time overlay of bright-field and near-infrared fluorescence images,” J. Biomed. Opt. 20(10), 106002 (2015).
[Crossref] [PubMed]

Rosenthal, E. L.

E. L. Rosenthal, B. D. Kulbersh, T. King, T. R. Chaudhuri, and K. R. Zinn, “Use of fluorescent labeled anti-epidermal growth factor receptor antibody to image head and neck squamous cell carcinoma xenografts,” Mol. Cancer Ther. 6(4), 1230–1238 (2007).
[Crossref] [PubMed]

Samkoe, K. S.

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

Sarantopoulos, A.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Schaafsma, B. E.

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

Skoch, J.

J. R. Watson, C. F. Gainer, N. Martirosyan, J. Skoch, G. M. Lemole, R. Anton, and M. Romanowski, “Augmented microscopy: real-time overlay of bright-field and near-infrared fluorescence images,” J. Biomed. Opt. 20(10), 106002 (2015).
[Crossref] [PubMed]

Sloan, A.

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

Stummer, W.

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,” Lancet Oncol. 7(5), 392–401 (2006).
[Crossref] [PubMed]

Themelis, G.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Tsien, R. Y.

Q. T. Nguyen and R. Y. Tsien, “Fluorescence-guided surgery with live molecular navigation--a new cutting edge,” Nat. Rev. Cancer 13(9), 653–662 (2013).
[Crossref] [PubMed]

Vahrmeijer, A. L.

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. 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] [PubMed]

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

Valdés, P. A.

P. A. Valdés, F. Leblond, V. L. Jacobs, B. C. Wilson, K. D. Paulsen, and D. W. Roberts, “Quantitative, spectrally-resolved intraoperative fluorescence imaging,” Sci. Rep. 2, 798 (2012).
[Crossref] [PubMed]

van Dam, G. M.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

van de Velde, C. J.

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. 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] [PubMed]

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

van der Vorst, J. R.

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. 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] [PubMed]

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

van der Zee, A. G.

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Watson, J. R.

J. R. Watson, C. F. Gainer, N. Martirosyan, J. Skoch, G. M. Lemole, R. Anton, and M. Romanowski, “Augmented microscopy: real-time overlay of bright-field and near-infrared fluorescence images,” J. Biomed. Opt. 20(10), 106002 (2015).
[Crossref] [PubMed]

Weis, J.

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

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,” Lancet Oncol. 7(5), 392–401 (2006).
[Crossref] [PubMed]

Wilson, B. C.

P. A. Valdés, F. Leblond, V. L. Jacobs, B. C. Wilson, K. D. Paulsen, and D. W. Roberts, “Quantitative, spectrally-resolved intraoperative fluorescence imaging,” Sci. Rep. 2, 798 (2012).
[Crossref] [PubMed]

Woyke, T.

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

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,” Lancet Oncol. 7(5), 392–401 (2006).
[Crossref] [PubMed]

Zinn, K. R.

E. L. Rosenthal, B. D. Kulbersh, T. King, T. R. Chaudhuri, and K. R. Zinn, “Use of fluorescent labeled anti-epidermal growth factor receptor antibody to image head and neck squamous cell carcinoma xenografts,” Mol. Cancer Ther. 6(4), 1230–1238 (2007).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

J. Biomed. Opt. (1)

J. R. Watson, C. F. Gainer, N. Martirosyan, J. Skoch, G. M. Lemole, R. Anton, and M. Romanowski, “Augmented microscopy: real-time overlay of bright-field and near-infrared fluorescence images,” J. Biomed. Opt. 20(10), 106002 (2015).
[Crossref] [PubMed]

J. Surg. Oncol. (1)

B. E. Schaafsma, J. S. Mieog, M. Hutteman, J. R. van der Vorst, P. J. Kuppen, C. W. Löwik, J. V. Frangioni, C. J. van de Velde, and A. L. Vahrmeijer, “The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery,” J. Surg. Oncol. 104(3), 323–332 (2011).
[Crossref] [PubMed]

Lancet Oncol. (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,” Lancet Oncol. 7(5), 392–401 (2006).
[Crossref] [PubMed]

Mol. Cancer Ther. (1)

E. L. Rosenthal, B. D. Kulbersh, T. King, T. R. Chaudhuri, and K. R. Zinn, “Use of fluorescent labeled anti-epidermal growth factor receptor antibody to image head and neck squamous cell carcinoma xenografts,” Mol. Cancer Ther. 6(4), 1230–1238 (2007).
[Crossref] [PubMed]

Nat. Med. (1)

G. M. van Dam, G. Themelis, L. M. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. Arts, A. G. van der Zee, J. Bart, P. S. Low, and V. Ntziachristos, “Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Nat. Rev. Cancer (1)

Q. T. Nguyen and R. Y. Tsien, “Fluorescence-guided surgery with live molecular navigation--a new cutting edge,” Nat. Rev. Cancer 13(9), 653–662 (2013).
[Crossref] [PubMed]

Nat. Rev. Clin. Oncol. (1)

A. L. Vahrmeijer, M. Hutteman, J. R. van der Vorst, C. J. 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] [PubMed]

Neoplasia (1)

D. B. Hoelzinger, L. Mariani, J. Weis, T. Woyke, T. J. Berens, W. S. McDonough, A. Sloan, S. W. Coons, and M. E. Berens, “Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets,” Neoplasia 7(1), 7–16 (2005).
[Crossref] [PubMed]

Sci. Rep. (1)

P. A. Valdés, F. Leblond, V. L. Jacobs, B. C. Wilson, K. D. Paulsen, and D. W. Roberts, “Quantitative, spectrally-resolved intraoperative fluorescence imaging,” Sci. Rep. 2, 798 (2012).
[Crossref] [PubMed]

Surg. Neurol. (1)

T. Kuroiwa, Y. Kajimoto, and T. Ohta, “Development of a fluorescein operative microscope for use during malignant glioma surgery: a technical note and preliminary report,” Surg. Neurol. 50(1), 41–49 (1998).
[Crossref] [PubMed]

Other (3)

A. V. Dsouza, H. Lin, E. R. Henderson, K. S. Samkoe, and B. W. Pogue, “Review of fluorescence guided surgery sytems: identification of key performance capabilities beyond indocyanine green imaging,” J. Biomed. Opt. (2016, Accepted July 19).

J. T. Elliott, K. Marra, L. T. Evans, S. C. Davis, K. S. Samkoe, J. D. Olson, J. Feldwisch, K. D. Paulsen, D. W. Roberts, and B. W. Pogue, “Simultaneous in vivo fluorescent markers for perfusion, protoporphyrin metabolism and EGFR expression for optically guided identification of orthotopic glioma,” Clin. Cancer Res.under review.

Food and Drug Administration, “Guidance for Industry, Investigators, and Reviewers: Exploratory IND Studies,” Office of Training and Communication HFD-240 (2006).

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Figures (4)

Fig. 1
Fig. 1

The detection module (blue) and the illumination model (yellow) are attached to the Zeiss Pentero OPMI head and can be used without affecting standard operation of the microscope.

Fig. 2
Fig. 2

(A) The laser (black line) is cleaned up by the ET770spuv shortpass filter before exiting the illumination module. This excitation along with coincident white-light from the Pentero is reflected by the T770lpxr dichroic towards the RGB camera. The fluorescence emission is transmitted through the dichroic and filtered by the ET780lp long-pass filter before sCMOS detection. (B) Maximum laser beam power, measured in the center of the illumination field was characterized using a power meter affixed with a 7-mm diameter aperture at different distances from the bottom of the adapter. The green shaded area indicates power per area below the ANSI limit for skin exposure for a continuous-wave 760 nm light source. The blue shaded area shows the typical working distance used during surgery. The IEC 3R Laser class limit is represented by the dashed grey line.

Fig. 3
Fig. 3

The relationship between signal and ABY-029 concentration for each system plotted on a log-log scale. When evaluating the microdose module, the Pentero xenon arc lamp was either off (squares) or on at 30% power (dots). Dashed lines show the line-of-best-fit over the linear response regions, and dotted lines show the noise floor. Black crosses show the intersection point which defines the lower limit of detection.

Fig. 4
Fig. 4

(A) The overlay (fusion) of two images acquired simultaneously during open craniotomy with the custom imaging module: the RGB white-light image and the fluorescence image overlay 2-h following a 3x microdose injection. (B) The ex vivo overlay of the whole brain acquired 2-h following a 6x microdose injection. (C) The corresponding ex vivo fluorescence image acquired with the Pentero IR800 channel. (D) A PpIX image acquired with the Zeiss Pentero BLUE400 channel, and (E) the same brain imaged by the custom imaging module during blue-light excitation. (F) The same brain as in D and E, imaged for ABY-029 fluorescence using the customized Pentero 2-h following a 3x microdose injection.

Tables (1)

Tables Icon

Table 1 The tumor to background ratio (TBR) and signal to noise ratio (SNR) determined for each dose level using each system. Values are group means with the 95% confidence interval of TBR indicated in parenthesis.

Metrics