Abstract

With the emergence of immunotherapies for cancer treatment, there is a rising clinical need to visualize the tumor microenvironment (TME) non-invasively in detail, which could be crucial to predict the efficacy of therapy. Nuclear imaging techniques enable whole-body imaging but lack the required spatial resolution. Conversely, near-infrared immunofluorescence (immuno-NIRF) is able to reveal tumor cells and/or other cell subsets in the TME by targeting the expression of a specific membrane receptor with fluorescently labeled monoclonal antibodies (mAb). Optical coherence tomography (OCT) provides three-dimensional morphological imaging of tissues without exogenous contrast agents. The combination of the two allows molecular and structural contrast at a resolution of ~15 µm, allowing for the specific location of a cell-type target with immuno-NIRF as well as revealing the three-dimensional architectural context with OCT. For the first time, combined immuno-NIRF and OCT of a tumor is demonstrated in situ in a xenograft mouse model of human colorectal cancer, targeted by a clinically-safe fluorescent mAb, revealing unprecedented details of the TME. A handheld scanner for ex vivo examination and an endoscope designed for imaging bronchioles in vivo are presented. This technique promises to complement nuclear imaging for diagnosing cancer invasiveness, precisely determining tumor margins, and studying the biodistribution of newly developed antibodies in high detail.

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

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2018 (1)

L. S. F. Boogerd, C. E. S. Hoogstins, D. P. Schaap, M. Kusters, H. J. M. Handgraaf, M. J. M. van der Valk, D. E. Hilling, F. A. Holman, K. C. M. J. Peeters, J. S. D. Mieog, C. J. H. van de Velde, A. Farina-Sarasqueta, I. van Lijnschoten, B. Framery, A. Pèlegrin, M. Gutowski, S. W. Nienhuijs, I. H. J. T. de Hingh, G. A. P. Nieuwenhuijzen, H. J. T. Rutten, F. Cailler, J. Burggraaf, and A. L. Vahrmeijer, “Safety and effectiveness of SGM-101, a fluorescent antibody targeting carcinoembryonic antigen, for intraoperative detection of colorectal cancer: a dose-escalation pilot study,” Lancet Gastroenterol. Hepatol. 3(3), 181–191 (2018).
[Crossref] [PubMed]

2017 (5)

R. R. Zhang, A. B. Schroeder, J. J. Grudzinski, E. L. Rosenthal, J. M. Warram, A. N. Pinchuk, K. W. Eliceiri, J. S. Kuo, and J. P. Weichert, “Beyond the margins: real-time detection of cancer using targeted fluorophores,” Nat. Rev. Clin. Oncol. 14(6), 347–364 (2017).
[Crossref] [PubMed]

M. Koch, J. S. de Jong, J. Glatz, P. Symvoulidis, L. E. Lamberts, A. L. L. Adams, M. E. G. Kranendonk, A. G. T. Terwisscha van Scheltinga, M. Aichler, L. Jansen, J. de Vries, M. N. Lub-de Hooge, C. P. Schröder, A. Jorritsma-Smit, M. D. Linssen, E. de Boer, B. van der Vegt, W. B. Nagengast, S. G. Elias, S. Oliveira, A. J. Witkamp, W. P. T. M. Mali, E. Van der Wall, P. B. Garcia-Allende, P. J. van Diest, E. G. E. de Vries, A. Walch, G. M. van Dam, and V. Ntziachristos, “Threshold Analysis and Biodistribution of Fluorescently Labeled Bevacizumab in Human Breast Cancer,” Cancer Res. 77(3), 623–631 (2017).
[Crossref] [PubMed]

A. A. Lammertsma, “Forward to the Past: The Case for Quantitative PET Imaging,” J. Nucl. Med. 58(7), 1019–1024 (2017).
[Crossref] [PubMed]

B. E. Sherlock, J. E. Phipps, J. Bec, and L. Marcu, “Simultaneous, label-free, multispectral fluorescence lifetime imaging and optical coherence tomography using a double-clad fiber,” Opt. Lett. 42(19), 3753–3756 (2017).
[Crossref] [PubMed]

M. Gao, F. Yu, C. Lv, J. Choo, and L. Chen, “Fluorescent chemical probes for accurate tumor diagnosis and targeting therapy,” Chem. Soc. Rev. 46(8), 2237–2271 (2017).
[Crossref] [PubMed]

2016 (3)

J. J. Tjalma, P. B. Garcia-Allende, E. Hartmans, A. G. Terwisscha van Scheltinga, W. Boersma-van Ek, J. Glatz, M. Koch, Y. J. van Herwaarden, T. M. Bisseling, I. D. Nagtegaal, H. Timmer-Bosscha, J. J. Koornstra, A. Karrenbeld, J. H. Kleibeuker, G. M. van Dam, V. Ntziachristos, and W. B. Nagengast, “Molecular Fluorescence Endoscopy Targeting Vascular Endothelial Growth Factor A for Improved Colorectal Polyp Detection,” J. Nucl. Med. 57(3), 480–485 (2016).
[Crossref] [PubMed]

R. Guay-Lord, X. Attendu, K. L. Lurie, L. Majeau, N. Godbout, A. K. E. Bowden, M. Strupler, and C. Boudoux, “Combined optical coherence tomography and hyperspectral imaging using a double-clad fiber coupler,” J. Biomed. Opt. 21(11), 116008 (2016).
[Crossref] [PubMed]

N. J. Harlaar, M. Koller, S. J. de Jongh, B. L. van Leeuwen, P. H. Hemmer, S. Kruijff, R. J. van Ginkel, L. B. Been, J. S. de Jong, G. Kats-Ugurlu, M. D. Linssen, A. Jorritsma-Smit, M. van Oosten, W. B. Nagengast, V. Ntziachristos, and G. M. van Dam, “Molecular fluorescence-guided surgery of peritoneal carcinomatosis of colorectal origin: a single-centre feasibility study,” Lancet Gastroenterol. Hepatol. 1(4), 283–290 (2016).
[Crossref] [PubMed]

2015 (8)

J. Li, F. Feroldi, J. de Lange, J. M. A. Daniels, K. Grünberg, and J. F. de Boer, “Polarization sensitive optical frequency domain imaging system for endobronchial imaging,” Opt. Express 23(3), 3390–3402 (2015).
[Crossref] [PubMed]

H. Wang, J. A. Gardecki, G. J. Ughi, P. V. Jacques, E. Hamidi, and G. J. Tearney, “Ex vivo catheter-based imaging of coronary atherosclerosis using multimodality OCT and NIRAF excited at 633 nm,” Biomed. Opt. Express 6(4), 1363–1375 (2015).
[Crossref] [PubMed]

M. C. Boonstra, B. Tolner, B. E. Schaafsma, L. S. F. Boogerd, H. A. J. M. Prevoo, G. Bhavsar, P. J. K. Kuppen, C. F. M. Sier, B. A. Bonsing, J. V. Frangioni, C. J. H. van de Velde, K. A. Chester, and A. L. Vahrmeijer, “Preclinical evaluation of a novel CEA-targeting near-infrared fluorescent tracer delineating colorectal and pancreatic tumors,” Int. J. Cancer 137(8), 1910–1920 (2015).
[Crossref] [PubMed]

K. Beaudette, H. W. Baac, W. J. Madore, M. Villiger, N. Godbout, B. E. Bouma, and C. Boudoux, “Laser tissue coagulation and concurrent optical coherence tomography through a double-clad fiber coupler,” Biomed. Opt. Express 6(4), 1293–1303 (2015).
[Crossref] [PubMed]

G. A. Van Dongen, M. C. Huisman, R. Boellaard, N. Harry Hendrikse, A. D. Windhorst, G. W. M. Visser, C. F. M. Molthoff, and D. J. Vugts, “89Zr-immuno-PET for imaging of long circulating drugs and disease targets: why, how and when to be applied?” Q. J. Nucl. Med. Mol. Imaging 59(1), 18–38 (2015).
[PubMed]

E. de Boer, N. J. Harlaar, A. Taruttis, W. B. Nagengast, E. L. Rosenthal, V. Ntziachristos, and G. M. van Dam, “Optical innovations in surgery,” Br. J. Surg. 102(2), e56–e72 (2015).
[Crossref] [PubMed]

E. L. Rosenthal, J. M. Warram, E. de Boer, T. K. Chung, M. L. Korb, M. Brandwein-Gensler, T. V. Strong, C. E. Schmalbach, A. B. Morlandt, G. Agarwal, Y. E. Hartman, W. R. Carroll, J. S. Richman, L. K. Clemons, L. M. Nabell, and K. R. Zinn, “Safety and Tumor Specificity of Cetuximab-IRDye800 for Surgical Navigation in Head and Neck Cancer,” Clin. Cancer Res. 21(16), 3658–3666 (2015).
[Crossref] [PubMed]

L. Scolaro, D. Lorenser, W. J. Madore, R. W. Kirk, A. S. Kramer, G. C. Yeoh, N. Godbout, D. D. Sampson, C. Boudoux, and R. A. McLaughlin, “Molecular imaging needles: dual-modality optical coherence tomography and fluorescence imaging of labeled antibodies deep in tissue,” Biomed. Opt. Express 6(5), 1767–1781 (2015).
[Crossref] [PubMed]

2014 (4)

H. Pahlevaninezhad, A. M. D. Lee, T. Shaipanich, R. Raizada, L. Cahill, G. Hohert, V. X. D. Yang, S. Lam, C. MacAulay, and P. Lane, “A high-efficiency fiber-based imaging system for co-registered autofluorescence and optical coherence tomography,” Biomed. Opt. Express 5(9), 2978–2987 (2014).
[Crossref] [PubMed]

S. Lee, M. W. Lee, H. S. Cho, J. W. Song, H. S. Nam, D. J. Oh, K. Park, W. Y. Oh, H. Yoo, and J. W. Kim, “Fully integrated high-speed intravascular optical coherence tomography/near-infrared fluorescence structural/molecular imaging in vivo using a clinically available near-infrared fluorescence-emitting indocyanine green to detect inflamed lipid-rich atheromata in coronary-sized vessels,” Circ. Cardiovasc. Interv. 7(4), 560–569 (2014).
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R. V. J. Chari, M. L. Miller, and W. C. Widdison, “Antibody-Drug Conjugates: An Emerging Concept in Cancer Therapy,” Angew. Chem. Int. Ed. Engl. 53(15), 3796–3827 (2014).
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S. Panowski, S. Bhakta, H. Raab, P. Polakis, and J. R. Junutula, “Site-specific antibody drug conjugates for cancer therapy,” MAbs 6(1), 34–45 (2014).
[Crossref] [PubMed]

2013 (6)

M. Hölzel, A. Bovier, and T. Tüting, “Plasticity of tumour and immune cells: a source of heterogeneity and a cause for therapy resistance?” Nat. Rev. Cancer 13(5), 365–376 (2013).
[Crossref] [PubMed]

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

D. Lorenser, B. C. Quirk, M. Auger, W. J. Madore, R. W. Kirk, N. Godbout, D. D. Sampson, C. Boudoux, and R. A. McLaughlin, “Dual-modality needle probe for combined fluorescence imaging and three-dimensional optical coherence tomography,” Opt. Lett. 38(3), 266–268 (2013).
[Crossref] [PubMed]

W. J. Madore, E. De Montigny, O. Ouellette, S. Lemire-Renaud, M. Leduc, X. Daxhelet, N. Godbout, and C. Boudoux, “Asymmetric double-clad fiber couplers for endoscopy,” Opt. Lett. 38(21), 4514–4517 (2013).
[Crossref] [PubMed]

R. Cohen, D. J. Vugts, M. Stigter-van Walsum, G. W. M. Visser, and G. A. M. S. van Dongen, “Inert coupling of IRDye800CW and zirconium-89 to monoclonal antibodies for single- or dual-mode fluorescence and PET imaging,” Nat. Protoc. 8(5), 1010–1018 (2013).
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A. M. Fard, P. Vacas-Jacques, E. Hamidi, H. Wang, R. W. Carruth, J. A. Gardecki, and G. J. Tearney, “Optical coherence tomography--near infrared spectroscopy system and catheter for intravascular imaging,” Opt. Express 21(25), 30849–30858 (2013).
[Crossref] [PubMed]

2012 (5)

2011 (5)

R. Cohen, M. A. Stammes, I. H. C. de Roos, M. Stigter-van Walsum, G. W. M. Visser, and G. A. van Dongen, “Inert coupling of IRDye800CW to monoclonal antibodies for clinical optical imaging of tumor targets,” EJNMMI Res. 1(1), 31 (2011).
[Crossref] [PubMed]

S. Goel, D. G. Duda, L. Xu, L. L. Munn, Y. Boucher, D. Fukumura, and R. K. Jain, “Normalization of the vasculature for treatment of cancer and other diseases,” Physiol. Rev. 91(3), 1071–1121 (2011).
[Crossref] [PubMed]

H. Yoo, J. W. Kim, M. Shishkov, E. Namati, T. Morse, R. Shubochkin, J. R. McCarthy, V. Ntziachristos, B. E. Bouma, F. A. Jaffer, and G. J. Tearney, “Intra-arterial catheter for simultaneous microstructural and molecular imaging in vivo,” Nat. Med. 17(12), 1680–1684 (2011).
[Crossref] [PubMed]

B. Braaf, K. A. Vermeer, V. A. Sicam, E. van Zeeburg, J. C. van Meurs, and J. F. de Boer, “Phase-stabilized optical frequency domain imaging at 1-µm for the measurement of blood flow in the human choroid,” Opt. Express 19(21), 20886–20903 (2011).
[Crossref] [PubMed]

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-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

2010 (1)

S. Yuan, C. A. Roney, J. Wierwille, C. W. Chen, B. Xu, G. Griffiths, J. Jiang, H. Ma, A. Cable, R. M. Summers, and Y. Chen, “Co-registered optical coherence tomography and fluorescence molecular imaging for simultaneous morphological and molecular imaging,” Phys. Med. Biol. 55(1), 191–206 (2010).
[Crossref] [PubMed]

2009 (1)

2008 (1)

2007 (1)

E. El Emir, U. Qureshi, J. L. J. Dearling, G. M. Boxer, I. Clatworthy, A. A. Folarin, M. P. Robson, S. Nagl, M. A. Konerding, and R. B. Pedley, “Predicting Response to Radioimmunotherapy from the Tumor Microenvironment of Colorectal Carcinomas,” Cancer Res. 67(24), 11896–11905 (2007).
[Crossref] [PubMed]

2006 (1)

E. L. Rosenthal, B. D. Kulbersh, R. D. Duncan, W. Zhang, J. S. Magnuson, W. R. Carroll, and K. Zinn, “In vivo detection of head and neck cancer orthotopic xenografts by immunofluorescence,” Laryngoscope 116(9), 1636–1641 (2006).
[Crossref] [PubMed]

2004 (1)

2003 (1)

J. V. Frangioni, “In vivo near-infrared fluorescence imaging,” Curr. Opin. Chem. Biol. 7(5), 626–634 (2003).
[Crossref] [PubMed]

2001 (1)

T. F. Chan and L. A. Vese, “Active contours without edges,” IEEE Trans. Image Process. 10(2), 266–277 (2001).
[Crossref] [PubMed]

1994 (1)

S. Folli, P. Westermann, D. Braichotte, A. Pèlegrin, G. Wagnières, H. van den Bergh, and J. P. Mach, “Antibody-indocyanin conjugates for immunophotodetection of human squamous cell carcinoma in nude mice,” Cancer Res. 54(10), 2643–2649 (1994).
[PubMed]

1993 (1)

H. J. Hansen, D. M. Goldenberg, E. S. Newman, R. Grebenau, and R. M. Sharkey, “Characterization of second-generation monoclonal antibodies against carcinoembryonic antigen,” Cancer 71(11), 3478–3485 (1993).
[Crossref] [PubMed]

1992 (1)

S. Folli, G. Wagnières, A. Pèlegrin, J. M. Calmes, D. Braichotte, F. Buchegger, Y. Chalandon, N. Hardman, C. Heusser, J. C. Givel, G. Chapuis, A. Chatelain, H. Vandenbergh, and J. P. Mach, “Immunophotodiagnosis of colon carcinomas in patients injected with fluoresceinated chimeric antibodies against carcinoembryonic antigen,” Proc. Natl. Acad. Sci. U.S.A. 89(17), 7973–7977 (1992).
[Crossref] [PubMed]

1991 (2)

A. Pèlegrin, S. Folli, F. Buchegger, J. P. Mach, G. Wagnières, and H. van den Bergh, “Antibody-fluorescein conjugates for photoimmunodiagnosis of human colon carcinoma in nude mice,” Cancer 67(10), 2529–2537 (1991).
[Crossref] [PubMed]

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

1959 (1)

E. W. Dijkstra, “A note on two problems in connexion with graphs,” Numer. Math. 1(1), 269–271 (1959).
[Crossref]

Adams, A. L. L.

M. Koch, J. S. de Jong, J. Glatz, P. Symvoulidis, L. E. Lamberts, A. L. L. Adams, M. E. G. Kranendonk, A. G. T. Terwisscha van Scheltinga, M. Aichler, L. Jansen, J. de Vries, M. N. Lub-de Hooge, C. P. Schröder, A. Jorritsma-Smit, M. D. Linssen, E. de Boer, B. van der Vegt, W. B. Nagengast, S. G. Elias, S. Oliveira, A. J. Witkamp, W. P. T. M. Mali, E. Van der Wall, P. B. Garcia-Allende, P. J. van Diest, E. G. E. de Vries, A. Walch, G. M. van Dam, and V. Ntziachristos, “Threshold Analysis and Biodistribution of Fluorescently Labeled Bevacizumab in Human Breast Cancer,” Cancer Res. 77(3), 623–631 (2017).
[Crossref] [PubMed]

Agarwal, G.

E. L. Rosenthal, J. M. Warram, E. de Boer, T. K. Chung, M. L. Korb, M. Brandwein-Gensler, T. V. Strong, C. E. Schmalbach, A. B. Morlandt, G. Agarwal, Y. E. Hartman, W. R. Carroll, J. S. Richman, L. K. Clemons, L. M. Nabell, and K. R. Zinn, “Safety and Tumor Specificity of Cetuximab-IRDye800 for Surgical Navigation in Head and Neck Cancer,” Clin. Cancer Res. 21(16), 3658–3666 (2015).
[Crossref] [PubMed]

Aichler, M.

M. Koch, J. S. de Jong, J. Glatz, P. Symvoulidis, L. E. Lamberts, A. L. L. Adams, M. E. G. Kranendonk, A. G. T. Terwisscha van Scheltinga, M. Aichler, L. Jansen, J. de Vries, M. N. Lub-de Hooge, C. P. Schröder, A. Jorritsma-Smit, M. D. Linssen, E. de Boer, B. van der Vegt, W. B. Nagengast, S. G. Elias, S. Oliveira, A. J. Witkamp, W. P. T. M. Mali, E. Van der Wall, P. B. Garcia-Allende, P. J. van Diest, E. G. E. de Vries, A. Walch, G. M. van Dam, and V. Ntziachristos, “Threshold Analysis and Biodistribution of Fluorescently Labeled Bevacizumab in Human Breast Cancer,” Cancer Res. 77(3), 623–631 (2017).
[Crossref] [PubMed]

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-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Attendu, X.

R. Guay-Lord, X. Attendu, K. L. Lurie, L. Majeau, N. Godbout, A. K. E. Bowden, M. Strupler, and C. Boudoux, “Combined optical coherence tomography and hyperspectral imaging using a double-clad fiber coupler,” J. Biomed. Opt. 21(11), 116008 (2016).
[Crossref] [PubMed]

Auger, M.

Baac, H. W.

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-α targeting: first in-human results,” Nat. Med. 17(10), 1315–1319 (2011).
[Crossref] [PubMed]

Barton, J. K.

Beaudette, K.

Bec, J.

Been, L. B.

N. J. Harlaar, M. Koller, S. J. de Jongh, B. L. van Leeuwen, P. H. Hemmer, S. Kruijff, R. J. van Ginkel, L. B. Been, J. S. de Jong, G. Kats-Ugurlu, M. D. Linssen, A. Jorritsma-Smit, M. van Oosten, W. B. Nagengast, V. Ntziachristos, and G. M. van Dam, “Molecular fluorescence-guided surgery of peritoneal carcinomatosis of colorectal origin: a single-centre feasibility study,” Lancet Gastroenterol. Hepatol. 1(4), 283–290 (2016).
[Crossref] [PubMed]

Bhakta, S.

S. Panowski, S. Bhakta, H. Raab, P. Polakis, and J. R. Junutula, “Site-specific antibody drug conjugates for cancer therapy,” MAbs 6(1), 34–45 (2014).
[Crossref] [PubMed]

Bhavsar, G.

M. C. Boonstra, B. Tolner, B. E. Schaafsma, L. S. F. Boogerd, H. A. J. M. Prevoo, G. Bhavsar, P. J. K. Kuppen, C. F. M. Sier, B. A. Bonsing, J. V. Frangioni, C. J. H. van de Velde, K. A. Chester, and A. L. Vahrmeijer, “Preclinical evaluation of a novel CEA-targeting near-infrared fluorescent tracer delineating colorectal and pancreatic tumors,” Int. J. Cancer 137(8), 1910–1920 (2015).
[Crossref] [PubMed]

Bisseling, T. M.

J. J. Tjalma, P. B. Garcia-Allende, E. Hartmans, A. G. Terwisscha van Scheltinga, W. Boersma-van Ek, J. Glatz, M. Koch, Y. J. van Herwaarden, T. M. Bisseling, I. D. Nagtegaal, H. Timmer-Bosscha, J. J. Koornstra, A. Karrenbeld, J. H. Kleibeuker, G. M. van Dam, V. Ntziachristos, and W. B. Nagengast, “Molecular Fluorescence Endoscopy Targeting Vascular Endothelial Growth Factor A for Improved Colorectal Polyp Detection,” J. Nucl. Med. 57(3), 480–485 (2016).
[Crossref] [PubMed]

Boellaard, R.

G. A. Van Dongen, M. C. Huisman, R. Boellaard, N. Harry Hendrikse, A. D. Windhorst, G. W. M. Visser, C. F. M. Molthoff, and D. J. Vugts, “89Zr-immuno-PET for imaging of long circulating drugs and disease targets: why, how and when to be applied?” Q. J. Nucl. Med. Mol. Imaging 59(1), 18–38 (2015).
[PubMed]

Boersma-van Ek, W.

J. J. Tjalma, P. B. Garcia-Allende, E. Hartmans, A. G. Terwisscha van Scheltinga, W. Boersma-van Ek, J. Glatz, M. Koch, Y. J. van Herwaarden, T. M. Bisseling, I. D. Nagtegaal, H. Timmer-Bosscha, J. J. Koornstra, A. Karrenbeld, J. H. Kleibeuker, G. M. van Dam, V. Ntziachristos, and W. B. Nagengast, “Molecular Fluorescence Endoscopy Targeting Vascular Endothelial Growth Factor A for Improved Colorectal Polyp Detection,” J. Nucl. Med. 57(3), 480–485 (2016).
[Crossref] [PubMed]

Bonsing, B. A.

M. C. Boonstra, B. Tolner, B. E. Schaafsma, L. S. F. Boogerd, H. A. J. M. Prevoo, G. Bhavsar, P. J. K. Kuppen, C. F. M. Sier, B. A. Bonsing, J. V. Frangioni, C. J. H. van de Velde, K. A. Chester, and A. L. Vahrmeijer, “Preclinical evaluation of a novel CEA-targeting near-infrared fluorescent tracer delineating colorectal and pancreatic tumors,” Int. J. Cancer 137(8), 1910–1920 (2015).
[Crossref] [PubMed]

Boogerd, L. S. F.

L. S. F. Boogerd, C. E. S. Hoogstins, D. P. Schaap, M. Kusters, H. J. M. Handgraaf, M. J. M. van der Valk, D. E. Hilling, F. A. Holman, K. C. M. J. Peeters, J. S. D. Mieog, C. J. H. van de Velde, A. Farina-Sarasqueta, I. van Lijnschoten, B. Framery, A. Pèlegrin, M. Gutowski, S. W. Nienhuijs, I. H. J. T. de Hingh, G. A. P. Nieuwenhuijzen, H. J. T. Rutten, F. Cailler, J. Burggraaf, and A. L. Vahrmeijer, “Safety and effectiveness of SGM-101, a fluorescent antibody targeting carcinoembryonic antigen, for intraoperative detection of colorectal cancer: a dose-escalation pilot study,” Lancet Gastroenterol. Hepatol. 3(3), 181–191 (2018).
[Crossref] [PubMed]

M. C. Boonstra, B. Tolner, B. E. Schaafsma, L. S. F. Boogerd, H. A. J. M. Prevoo, G. Bhavsar, P. J. K. Kuppen, C. F. M. Sier, B. A. Bonsing, J. V. Frangioni, C. J. H. van de Velde, K. A. Chester, and A. L. Vahrmeijer, “Preclinical evaluation of a novel CEA-targeting near-infrared fluorescent tracer delineating colorectal and pancreatic tumors,” Int. J. Cancer 137(8), 1910–1920 (2015).
[Crossref] [PubMed]

Boonstra, M. C.

M. C. Boonstra, B. Tolner, B. E. Schaafsma, L. S. F. Boogerd, H. A. J. M. Prevoo, G. Bhavsar, P. J. K. Kuppen, C. F. M. Sier, B. A. Bonsing, J. V. Frangioni, C. J. H. van de Velde, K. A. Chester, and A. L. Vahrmeijer, “Preclinical evaluation of a novel CEA-targeting near-infrared fluorescent tracer delineating colorectal and pancreatic tumors,” Int. J. Cancer 137(8), 1910–1920 (2015).
[Crossref] [PubMed]

Boucher, Y.

S. Goel, D. G. Duda, L. Xu, L. L. Munn, Y. Boucher, D. Fukumura, and R. K. Jain, “Normalization of the vasculature for treatment of cancer and other diseases,” Physiol. Rev. 91(3), 1071–1121 (2011).
[Crossref] [PubMed]

Boudoux, C.

Bouma, B. E.

K. Beaudette, H. W. Baac, W. J. Madore, M. Villiger, N. Godbout, B. E. Bouma, and C. Boudoux, “Laser tissue coagulation and concurrent optical coherence tomography through a double-clad fiber coupler,” Biomed. Opt. Express 6(4), 1293–1303 (2015).
[Crossref] [PubMed]

B. J. Vakoc, D. Fukumura, R. K. Jain, and B. E. Bouma, “Cancer imaging by optical coherence tomography: preclinical progress and clinical potential,” Nat. Rev. Cancer 12(5), 363–368 (2012).
[Crossref] [PubMed]

H. Yoo, J. W. Kim, M. Shishkov, E. Namati, T. Morse, R. Shubochkin, J. R. McCarthy, V. Ntziachristos, B. E. Bouma, F. A. Jaffer, and G. J. Tearney, “Intra-arterial catheter for simultaneous microstructural and molecular imaging in vivo,” Nat. Med. 17(12), 1680–1684 (2011).
[Crossref] [PubMed]

Bovier, A.

M. Hölzel, A. Bovier, and T. Tüting, “Plasticity of tumour and immune cells: a source of heterogeneity and a cause for therapy resistance?” Nat. Rev. Cancer 13(5), 365–376 (2013).
[Crossref] [PubMed]

Bowden, A. K. E.

R. Guay-Lord, X. Attendu, K. L. Lurie, L. Majeau, N. Godbout, A. K. E. Bowden, M. Strupler, and C. Boudoux, “Combined optical coherence tomography and hyperspectral imaging using a double-clad fiber coupler,” J. Biomed. Opt. 21(11), 116008 (2016).
[Crossref] [PubMed]

Boxer, G. M.

E. El Emir, U. Qureshi, J. L. J. Dearling, G. M. Boxer, I. Clatworthy, A. A. Folarin, M. P. Robson, S. Nagl, M. A. Konerding, and R. B. Pedley, “Predicting Response to Radioimmunotherapy from the Tumor Microenvironment of Colorectal Carcinomas,” Cancer Res. 67(24), 11896–11905 (2007).
[Crossref] [PubMed]

Braaf, B.

Braichotte, D.

S. Folli, P. Westermann, D. Braichotte, A. Pèlegrin, G. Wagnières, H. van den Bergh, and J. P. Mach, “Antibody-indocyanin conjugates for immunophotodetection of human squamous cell carcinoma in nude mice,” Cancer Res. 54(10), 2643–2649 (1994).
[PubMed]

S. Folli, G. Wagnières, A. Pèlegrin, J. M. Calmes, D. Braichotte, F. Buchegger, Y. Chalandon, N. Hardman, C. Heusser, J. C. Givel, G. Chapuis, A. Chatelain, H. Vandenbergh, and J. P. Mach, “Immunophotodiagnosis of colon carcinomas in patients injected with fluoresceinated chimeric antibodies against carcinoembryonic antigen,” Proc. Natl. Acad. Sci. U.S.A. 89(17), 7973–7977 (1992).
[Crossref] [PubMed]

Brandwein-Gensler, M.

E. L. Rosenthal, J. M. Warram, E. de Boer, T. K. Chung, M. L. Korb, M. Brandwein-Gensler, T. V. Strong, C. E. Schmalbach, A. B. Morlandt, G. Agarwal, Y. E. Hartman, W. R. Carroll, J. S. Richman, L. K. Clemons, L. M. Nabell, and K. R. Zinn, “Safety and Tumor Specificity of Cetuximab-IRDye800 for Surgical Navigation in Head and Neck Cancer,” Clin. Cancer Res. 21(16), 3658–3666 (2015).
[Crossref] [PubMed]

Buchegger, F.

S. Folli, G. Wagnières, A. Pèlegrin, J. M. Calmes, D. Braichotte, F. Buchegger, Y. Chalandon, N. Hardman, C. Heusser, J. C. Givel, G. Chapuis, A. Chatelain, H. Vandenbergh, and J. P. Mach, “Immunophotodiagnosis of colon carcinomas in patients injected with fluoresceinated chimeric antibodies against carcinoembryonic antigen,” Proc. Natl. Acad. Sci. U.S.A. 89(17), 7973–7977 (1992).
[Crossref] [PubMed]

A. Pèlegrin, S. Folli, F. Buchegger, J. P. Mach, G. Wagnières, and H. van den Bergh, “Antibody-fluorescein conjugates for photoimmunodiagnosis of human colon carcinoma in nude mice,” Cancer 67(10), 2529–2537 (1991).
[Crossref] [PubMed]

Burggraaf, J.

L. S. F. Boogerd, C. E. S. Hoogstins, D. P. Schaap, M. Kusters, H. J. M. Handgraaf, M. J. M. van der Valk, D. E. Hilling, F. A. Holman, K. C. M. J. Peeters, J. S. D. Mieog, C. J. H. van de Velde, A. Farina-Sarasqueta, I. van Lijnschoten, B. Framery, A. Pèlegrin, M. Gutowski, S. W. Nienhuijs, I. H. J. T. de Hingh, G. A. P. Nieuwenhuijzen, H. J. T. Rutten, F. Cailler, J. Burggraaf, and A. L. Vahrmeijer, “Safety and effectiveness of SGM-101, a fluorescent antibody targeting carcinoembryonic antigen, for intraoperative detection of colorectal cancer: a dose-escalation pilot study,” Lancet Gastroenterol. Hepatol. 3(3), 181–191 (2018).
[Crossref] [PubMed]

Cable, A.

S. Yuan, C. A. Roney, J. Wierwille, C. W. Chen, B. Xu, G. Griffiths, J. Jiang, H. Ma, A. Cable, R. M. Summers, and Y. Chen, “Co-registered optical coherence tomography and fluorescence molecular imaging for simultaneous morphological and molecular imaging,” Phys. Med. Biol. 55(1), 191–206 (2010).
[Crossref] [PubMed]

Cahill, L.

Cailler, F.

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Saidi, A.

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E. L. Rosenthal, J. M. Warram, E. de Boer, T. K. Chung, M. L. Korb, M. Brandwein-Gensler, T. V. Strong, C. E. Schmalbach, A. B. Morlandt, G. Agarwal, Y. E. Hartman, W. R. Carroll, J. S. Richman, L. K. Clemons, L. M. Nabell, and K. R. Zinn, “Safety and Tumor Specificity of Cetuximab-IRDye800 for Surgical Navigation in Head and Neck Cancer,” Clin. Cancer Res. 21(16), 3658–3666 (2015).
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Supplementary Material (3)

NameDescription
» Visualization 1       Fig 6 video. Sequence of OCT cross sections and 1D antibody-mediated NIRF, acquired simultaneosuly from a colon cancer mouse model with a galvo based scanner. Scale bar is 200 µm. Video rate 24 fps
» Visualization 2       Fig 7 video. Sequence of OCT cross sections and 1D antibody-mediated NIRF, acquired simultaneosuly from a colon cancer mouse model with a galvo based scanner. Scale bar is 100 µm. Video rate 24 fps
» Visualization 3       Fig 8 video. The video shows the sequence of cross-sectional OCT (B-scans) and one-dimensional NIRF that were simultaneously acquired.The tumor locations are identified by high immuno-NIRF signal (green lines). Fig 8 video. Distance between markers

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Figures (8)

Fig. 1
Fig. 1 The optical system combines a single-mode fiber-based swept-source 1310 nm OCT setup with an all-fiber fluorescence system based on continuous wave (CW) excitation at 780 nm. The OCT system is based on a modified Mach-Zehnder interferometer that features a circulator (C) in the sample arm for increased sensitivity and a polarization diversity detection module (PDDM) that splits the interference signals into S and P polarizations before balanced detection. FBG: Fiber Bragg Grating, PC: Polarization Controller, DAQ: Data Acquisition Card. An SMF-28 based wavelength division multiplexer (WDM) combines the OCT light with the fluorescence excitation light of a bandpass filtered (BP) CW laser (780 nm). A double-clad fiber (DCF) coupler delivers the light to the sample, and ensures that the backscattered OCT light travels back to the interferometer through its single-mode core. Conversely, the collected cladding light is extracted into a multimode fiber (MM), filtered by a short-pass filter (SP) and a long-pass filter (LP) to select the emission band of the fluorophore, and finally detected by a single photon avalanche photodiode (SPAD). The DCF coupler can be connected to either an endoscope (i) for imaging internal organs or a galvo-based scanner (ii) to image ex vivo samples or externally accessible organs. The imaging endoscope features a micromotor at the tip to scan the beam circumferentially. The galvo-based “handheld” scanner is composed of a reflective collimator to minimize focal shifts between the different wavelengths, an X-Y galvo scanner pair, and an objective to deliver the light to and collect the light from the sample.
Fig. 2
Fig. 2 a) Schematic representation of the DCF-based endoscope. A GRIN lens focuses the light that is transmitted by the single-mode core and scanned circularly by a motorized micromirror. The backscattered light is collected by both the single-mode core and the inner cladding of the DCF. b) photo of the tip of the endoscope. Distance between markers on the ruler is 0.5 mm.
Fig. 3
Fig. 3 a) The 780 nm laser excitation linewidth (solid blue), the spectrum of the photoluminescence in silica DCF fiber (dashed-dotted blue), and the emission spectrum of [89Zr]Zr-labetuzumab-IRDye800CW (dotted blue) are shown on a normalized intensity scale. In orange the transmission curves of the optical filters; BLP785R (dashed orange), BLP830RE longpass filter (dashed-dotted orange), and shortpass filter SH900 (solid orange). b) The measured intensity of the photoluminescence for DCF segments of increasing length (blue dots), normalized by the injected optical power, versus a linear-model weighted fitted line (orange solid line). The error bars are not shown because they are too small to be visible.
Fig. 4
Fig. 4 Log-log plot of the NIRF setup SNR. a) NIRF SNR with the galvo-based scanner in the range 0.3 nM to 30 nM, shown on a logarithmic scale. b) NIRF SNR of the endoscope, in the range 10 nM to 1 µM, shown on a logarithmic scale. The green dots represent the measurements done with filter BLP830RE, while the orange dots the ones done with filter BLP785R. The narrow band filter BLP830RE ensures higher signal-to-noise ratio for both scanners, over the whole range of concentrations.
Fig. 5
Fig. 5 a) PET-CT image of a mouse bearing LS174T colon cancer xenografts i.p. b) A wide-field NIR fluorescence image of the same mouse showing the accumulation of [89Zr]Zr-labetuzumab-IRDye800CW i.p. The greyscale range is [5.0–12]∙106 photons/s∙mm2. c) The large tumor visible in images (a) and (b) was excised and imaged again ex vivo with the wide-field NIR fluorescence imager. The color-scale range is [4.2–58]∙106 photons/s∙mm2. (i.e. fluorescence background and maximum value). d) The same excised tumor imaged with our custom NIRF scanner. The tumor was imaged from the opposite side with respect to the wide-field NIR fluorescence imager. The grayscale ranges from the background count rate to 0.8 times the maximum count rate of the image, in numbers: [1.8–21.6]∙106 photons/s. e) Zoomed in view of the area marked by the red square in (d) showing heterogeneity of the tumor. The connective tissue appears as white (low-fluorescence) areas. The greyscale range is [1.8–21.6]∙106 photons/s. All scale bars are 500 µm.
Fig. 6
Fig. 6 a) En face (coronal) NIRF image of a tumor located next to the liver of the mouse, which is visible on the left side of the image. The tumor is delineated by the orange contour, segmented with a Chen-Vese algorithm, which was used to increase the precision of the OCT segmentation by isolating the tumor portions from the B-scans. The greyscale range is [0.8–9.4]∙106 photons/s (i.e. fluorescence background and 0.8 times the maximum value). b) En face OCT projection obtained by integrating OCT intensity over a depth of 880 µm starting from the tissue surface. The liver is visible on the left side of the image. The tumor is delineated by the orange contour obtained from a). c-f) 1-D NIRF and OCT cross sections of the locations marked by the green lines in a) and the black lines in b). The liver structure is remarkably different from the tumor, which shows a higher degree of heterogeneity. Other tissue that was not labeled by the mAb is visible on the right side of image f). The OCT greyscale dynamic range is 55 dB. The tissue surface was segmented from the OCT B-scans with an automated algorithm, which separated areas of tumor from other tissues because the tumor protruded significantly from the rest of the sample. Scale bars are 200 µm (Visualization 1).
Fig. 7
Fig. 7 In situ NIRF and OCT images of a tumor located on top of the spleen of one of the mice of the study. a) NIRF image of a tumor mass, showing that tumors developed in several lobes. The tumor is delineated by the orange contour, segmented with a Chen-Vese algorithm. The greyscale range is [2.2–26.0]∙106 photons/s (i.e. fluorescence background and 0.8 times the maximum value). b) en face (coronal) projection of the OCT scan constructed by integrating the C-scan over a depth of 700 µm starting from the tissue surface. The tumor is delineated by the orange contour obtained from a). c-f) 1-D NIRF and OCT B-scans corresponding to the locations marked with the green lines in a) and black lines in b). The OCT greyscale dynamic range is 55 dB. Scale bars are 100 µm (Visualization 2).
Fig. 8
Fig. 8 Combined NIRF and OCT endoscopic images of a tumor located in the peritoneal cavity. a) and b) show NIRF and en face OCT images of the tumor, respectively, unwrapped along the circumference of the endoscope. The NIRF greyscale range is [1.1–3.5]∙106 photons/s (i.e. fluorescence background and maximum value). The en face OCT projection was obtained by integrating OCT intensity over a depth of 500 µm starting from the tissue surface. The vertical axis represents the circumference of the endoscope, the horizontal axis represents the pullback direction over a distance of 5 mm, from left to right. Scale bars 200 µm. The tumor is delineated by the orange contour obtained similarly to Fig. (7) and 8. Figs. (c-h) show cross sectional images taken from sequential locations along the pullback, indicated by the vertical green lines in a) and the black lines in b), from left to right. The inner circles show the one-dimensional NIRF data surrounded by the OCT cross sections segmented starting from the endoscope outer sheath. The white wedge of each B-scan masks the area of tissue blocked by the electrical wires. Distance between markers 0.5 mm (Visualization 3).

Equations (1)

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SNR=10 log 10 ( SB σ B )

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