Abstract

Minimally-invasive surgery of hepatocellular carcinoma (HCC) can be limited by poor tumor visualization with white light. We demonstrate systemic administration of a Cy5.5-labeled peptide specific for epidermal growth factor receptor (EGFR) to target HCC in vivo in a mouse xenograft model. We attached a compact imaging module to the proximal end of a medical laparoscope to collect near-infrared fluorescence and reflectance images concurrently at 15 frames/sec. We measured a mean target-to-background ratio of 2.99 ± 0.22 from 13 surgically exposed subcutaneous human HCC tumors in vivo in 5 mice. This integrated imaging methodology is promising to guide laparoscopic resection of HCC.

© 2016 Optical Society of America

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  1. A. P. Venook, C. Papandreou, J. Furuse, and L. L. de Guevara, “The incidence and epidemiology of hepatocellular carcinoma: a global and regional perspective,” Oncologist 15(Suppl 4), 5–13 (2010).
    [Crossref] [PubMed]
  2. J. M. Llovet, M. Schwartz, and V. Mazzaferro, “Resection and liver transplantation for hepatocellular carcinoma,” Semin. Liver Dis. 25(2), 181–200 (2005).
    [Crossref] [PubMed]
  3. I. Dagher, P. Lainas, A. Carloni, C. Caillard, A. Champault, C. Smadja, and D. Franco, “Laparoscopic liver resection for hepatocellular carcinoma,” Surg. Endosc. 22(2), 372–378 (2008).
    [Crossref] [PubMed]
  4. C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
    [Crossref] [PubMed]
  5. Y. Chen, X. Intes, and B. Chance, “Development of high-sensitivity near-infrared fluorescence imaging device for early cancer detection,” Biomed. Instrum. Technol. 39(1), 75–85 (2005).
    [PubMed]
  6. G. M. Thurber, M. M. Schmidt, and K. D. Wittrup, “Antibody tumor penetration: transport opposed by systemic and antigen-mediated clearance,” Adv. Drug Deliv. Rev. 60(12), 1421–1434 (2008).
    [Crossref] [PubMed]
  7. S. Lee, J. Xie, and X. Chen, “Peptides and peptide hormones for molecular imaging and disease diagnosis,” Chem. Rev. 110(5), 3087–3111 (2010).
    [Crossref] [PubMed]
  8. P. Huang, X. Xu, L. Wang, B. Zhu, X. Wang, and J. Xia, “The role of EGF-EGFR signalling pathway in hepatocellular carcinoma inflammatory microenvironment,” J. Cell. Mol. Med. 18(2), 218–230 (2014).
    [Crossref] [PubMed]
  9. A. F. Buckley, L. J. Burgart, V. Sahai, and S. Kakar, “Epidermal growth factor receptor expression and gene copy number in conventional hepatocellular carcinoma,” Am. J. Clin. Pathol. 129(2), 245–251 (2008).
    [Crossref] [PubMed]
  10. J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
    [Crossref] [PubMed]
  11. Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
    [PubMed]
  12. M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
    [Crossref] [PubMed]
  13. T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
    [Crossref] [PubMed]
  14. T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
    [Crossref]
  15. Venugopal V, Park M, Ashitate Y, Neacsu F, Kettenring F, Frangioni JV, Gangadharan SP, Gioux S. Design and characterization of an optimized simultaneous color and near-infrared fluorescence rigid endoscopic imaging system. J Biomed Opt 2013;18:126018.1.

2016 (1)

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

2015 (2)

J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
[Crossref] [PubMed]

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

2014 (2)

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

P. Huang, X. Xu, L. Wang, B. Zhu, X. Wang, and J. Xia, “The role of EGF-EGFR signalling pathway in hepatocellular carcinoma inflammatory microenvironment,” J. Cell. Mol. Med. 18(2), 218–230 (2014).
[Crossref] [PubMed]

2010 (4)

A. P. Venook, C. Papandreou, J. Furuse, and L. L. de Guevara, “The incidence and epidemiology of hepatocellular carcinoma: a global and regional perspective,” Oncologist 15(Suppl 4), 5–13 (2010).
[Crossref] [PubMed]

T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
[Crossref]

S. Lee, J. Xie, and X. Chen, “Peptides and peptide hormones for molecular imaging and disease diagnosis,” Chem. Rev. 110(5), 3087–3111 (2010).
[Crossref] [PubMed]

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

2008 (3)

A. F. Buckley, L. J. Burgart, V. Sahai, and S. Kakar, “Epidermal growth factor receptor expression and gene copy number in conventional hepatocellular carcinoma,” Am. J. Clin. Pathol. 129(2), 245–251 (2008).
[Crossref] [PubMed]

I. Dagher, P. Lainas, A. Carloni, C. Caillard, A. Champault, C. Smadja, and D. Franco, “Laparoscopic liver resection for hepatocellular carcinoma,” Surg. Endosc. 22(2), 372–378 (2008).
[Crossref] [PubMed]

G. M. Thurber, M. M. Schmidt, and K. D. Wittrup, “Antibody tumor penetration: transport opposed by systemic and antigen-mediated clearance,” Adv. Drug Deliv. Rev. 60(12), 1421–1434 (2008).
[Crossref] [PubMed]

2005 (2)

J. M. Llovet, M. Schwartz, and V. Mazzaferro, “Resection and liver transplantation for hepatocellular carcinoma,” Semin. Liver Dis. 25(2), 181–200 (2005).
[Crossref] [PubMed]

Y. Chen, X. Intes, and B. Chance, “Development of high-sensitivity near-infrared fluorescence imaging device for early cancer detection,” Biomed. Instrum. Technol. 39(1), 75–85 (2005).
[PubMed]

Abo, T.

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Aoki, T.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Arai, J.

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Azoulay, D.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Bandai, Y.

T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
[Crossref]

Buckley, A. F.

A. F. Buckley, L. J. Burgart, V. Sahai, and S. Kakar, “Epidermal growth factor receptor expression and gene copy number in conventional hepatocellular carcinoma,” Am. J. Clin. Pathol. 129(2), 245–251 (2008).
[Crossref] [PubMed]

Burgart, L. J.

A. F. Buckley, L. J. Burgart, V. Sahai, and S. Kakar, “Epidermal growth factor receptor expression and gene copy number in conventional hepatocellular carcinoma,” Am. J. Clin. Pathol. 129(2), 245–251 (2008).
[Crossref] [PubMed]

Caillard, C.

I. Dagher, P. Lainas, A. Carloni, C. Caillard, A. Champault, C. Smadja, and D. Franco, “Laparoscopic liver resection for hepatocellular carcinoma,” Surg. Endosc. 22(2), 372–378 (2008).
[Crossref] [PubMed]

Carloni, A.

I. Dagher, P. Lainas, A. Carloni, C. Caillard, A. Champault, C. Smadja, and D. Franco, “Laparoscopic liver resection for hepatocellular carcinoma,” Surg. Endosc. 22(2), 372–378 (2008).
[Crossref] [PubMed]

Champault, A.

I. Dagher, P. Lainas, A. Carloni, C. Caillard, A. Champault, C. Smadja, and D. Franco, “Laparoscopic liver resection for hepatocellular carcinoma,” Surg. Endosc. 22(2), 372–378 (2008).
[Crossref] [PubMed]

Chance, B.

Y. Chen, X. Intes, and B. Chance, “Development of high-sensitivity near-infrared fluorescence imaging device for early cancer detection,” Biomed. Instrum. Technol. 39(1), 75–85 (2005).
[PubMed]

Chen, X.

S. Lee, J. Xie, and X. Chen, “Peptides and peptide hormones for molecular imaging and disease diagnosis,” Chem. Rev. 110(5), 3087–3111 (2010).
[Crossref] [PubMed]

Chen, Y.

Y. Chen, X. Intes, and B. Chance, “Development of high-sensitivity near-infrared fluorescence imaging device for early cancer detection,” Biomed. Instrum. Technol. 39(1), 75–85 (2005).
[PubMed]

Dagher, I.

I. Dagher, P. Lainas, A. Carloni, C. Caillard, A. Champault, C. Smadja, and D. Franco, “Laparoscopic liver resection for hepatocellular carcinoma,” Surg. Endosc. 22(2), 372–378 (2008).
[Crossref] [PubMed]

de Guevara, L. L.

A. P. Venook, C. Papandreou, J. Furuse, and L. L. de Guevara, “The incidence and epidemiology of hepatocellular carcinoma: a global and regional perspective,” Oncologist 15(Suppl 4), 5–13 (2010).
[Crossref] [PubMed]

Delaney, P.

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

Duan, X.

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
[Crossref] [PubMed]

Foersch, S.

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

Franco, D.

I. Dagher, P. Lainas, A. Carloni, C. Caillard, A. Champault, C. Smadja, and D. Franco, “Laparoscopic liver resection for hepatocellular carcinoma,” Surg. Endosc. 22(2), 372–378 (2008).
[Crossref] [PubMed]

Furuse, J.

A. P. Venook, C. Papandreou, J. Furuse, and L. L. de Guevara, “The incidence and epidemiology of hepatocellular carcinoma: a global and regional perspective,” Oncologist 15(Suppl 4), 5–13 (2010).
[Crossref] [PubMed]

Galle, P. R.

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

Goetz, M.

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

Harada, N.

T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
[Crossref]

Hasegawa, K.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Hidaka, S.

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Huang, P.

P. Huang, X. Xu, L. Wang, B. Zhu, X. Wang, and J. Xia, “The role of EGF-EGFR signalling pathway in hepatocellular carcinoma inflammatory microenvironment,” J. Cell. Mol. Med. 18(2), 218–230 (2014).
[Crossref] [PubMed]

Ijichi, M.

T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
[Crossref]

Intes, X.

Y. Chen, X. Intes, and B. Chance, “Development of high-sensitivity near-infrared fluorescence imaging device for early cancer detection,” Biomed. Instrum. Technol. 39(1), 75–85 (2005).
[PubMed]

Ishizawa, T.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
[Crossref]

Joshi, B. P.

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
[Crossref] [PubMed]

Kakar, S.

A. F. Buckley, L. J. Burgart, V. Sahai, and S. Kakar, “Epidermal growth factor receptor expression and gene copy number in conventional hepatocellular carcinoma,” Am. J. Clin. Pathol. 129(2), 245–251 (2008).
[Crossref] [PubMed]

Kiesslich, R.

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

Kokudo, N.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
[Crossref]

Kuick, R.

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
[Crossref] [PubMed]

Kusaka, K.

T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
[Crossref]

Lainas, P.

I. Dagher, P. Lainas, A. Carloni, C. Caillard, A. Champault, C. Smadja, and D. Franco, “Laparoscopic liver resection for hepatocellular carcinoma,” Surg. Endosc. 22(2), 372–378 (2008).
[Crossref] [PubMed]

Lee, S.

S. Lee, J. Xie, and X. Chen, “Peptides and peptide hormones for molecular imaging and disease diagnosis,” Chem. Rev. 110(5), 3087–3111 (2010).
[Crossref] [PubMed]

Li, G.

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

Li, Z.

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

Lim, C.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Llovet, J. M.

J. M. Llovet, M. Schwartz, and V. Mazzaferro, “Resection and liver transplantation for hepatocellular carcinoma,” Semin. Liver Dis. 25(2), 181–200 (2005).
[Crossref] [PubMed]

Mazzaferro, V.

J. M. Llovet, M. Schwartz, and V. Mazzaferro, “Resection and liver transplantation for hepatocellular carcinoma,” Semin. Liver Dis. 25(2), 181–200 (2005).
[Crossref] [PubMed]

Mise, Y.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Miyaaki, H.

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Muraoka, A.

T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
[Crossref]

Nagayasu, T.

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Nanashima, A.

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Neurath, M. F.

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

Owens, S. R.

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
[Crossref] [PubMed]

Pant, A.

J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
[Crossref] [PubMed]

Papandreou, C.

A. P. Venook, C. Papandreou, J. Furuse, and L. L. de Guevara, “The incidence and epidemiology of hepatocellular carcinoma: a global and regional perspective,” Oncologist 15(Suppl 4), 5–13 (2010).
[Crossref] [PubMed]

Qiu, Z.

J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
[Crossref] [PubMed]

Sahai, V.

A. F. Buckley, L. J. Burgart, V. Sahai, and S. Kakar, “Epidermal growth factor receptor expression and gene copy number in conventional hepatocellular carcinoma,” Am. J. Clin. Pathol. 129(2), 245–251 (2008).
[Crossref] [PubMed]

Sakamoto, Y.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Salloum, C.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Schmidt, M. M.

G. M. Thurber, M. M. Schmidt, and K. D. Wittrup, “Antibody tumor penetration: transport opposed by systemic and antigen-mediated clearance,” Adv. Drug Deliv. Rev. 60(12), 1421–1434 (2008).
[Crossref] [PubMed]

Schwartz, M.

J. M. Llovet, M. Schwartz, and V. Mazzaferro, “Resection and liver transplantation for hepatocellular carcinoma,” Semin. Liver Dis. 25(2), 181–200 (2005).
[Crossref] [PubMed]

Shibasaki, M.

T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
[Crossref]

Shibata, H.

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Smadja, C.

I. Dagher, P. Lainas, A. Carloni, C. Caillard, A. Champault, C. Smadja, and D. Franco, “Laparoscopic liver resection for hepatocellular carcinoma,” Surg. Endosc. 22(2), 372–378 (2008).
[Crossref] [PubMed]

Sugawara, Y.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Takagi, K.

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Taura, N.

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Thurber, G. M.

G. M. Thurber, M. M. Schmidt, and K. D. Wittrup, “Antibody tumor penetration: transport opposed by systemic and antigen-mediated clearance,” Adv. Drug Deliv. Rev. 60(12), 1421–1434 (2008).
[Crossref] [PubMed]

Tobinaga, S.

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Venook, A. P.

A. P. Venook, C. Papandreou, J. Furuse, and L. L. de Guevara, “The incidence and epidemiology of hepatocellular carcinoma: a global and regional perspective,” Oncologist 15(Suppl 4), 5–13 (2010).
[Crossref] [PubMed]

Vibert, E.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Vieth, M.

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

Waldner, M. J.

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

Wang, L.

P. Huang, X. Xu, L. Wang, B. Zhu, X. Wang, and J. Xia, “The role of EGF-EGFR signalling pathway in hepatocellular carcinoma inflammatory microenvironment,” J. Cell. Mol. Med. 18(2), 218–230 (2014).
[Crossref] [PubMed]

Wang, T. D.

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
[Crossref] [PubMed]

Wang, X.

P. Huang, X. Xu, L. Wang, B. Zhu, X. Wang, and J. Xia, “The role of EGF-EGFR signalling pathway in hepatocellular carcinoma inflammatory microenvironment,” J. Cell. Mol. Med. 18(2), 218–230 (2014).
[Crossref] [PubMed]

Wittrup, K. D.

G. M. Thurber, M. M. Schmidt, and K. D. Wittrup, “Antibody tumor penetration: transport opposed by systemic and antigen-mediated clearance,” Adv. Drug Deliv. Rev. 60(12), 1421–1434 (2008).
[Crossref] [PubMed]

Xia, J.

P. Huang, X. Xu, L. Wang, B. Zhu, X. Wang, and J. Xia, “The role of EGF-EGFR signalling pathway in hepatocellular carcinoma inflammatory microenvironment,” J. Cell. Mol. Med. 18(2), 218–230 (2014).
[Crossref] [PubMed]

Xie, J.

S. Lee, J. Xie, and X. Chen, “Peptides and peptide hormones for molecular imaging and disease diagnosis,” Chem. Rev. 110(5), 3087–3111 (2010).
[Crossref] [PubMed]

Xu, X.

P. Huang, X. Xu, L. Wang, B. Zhu, X. Wang, and J. Xia, “The role of EGF-EGFR signalling pathway in hepatocellular carcinoma inflammatory microenvironment,” J. Cell. Mol. Med. 18(2), 218–230 (2014).
[Crossref] [PubMed]

Yoshioka, R.

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Zhou, J.

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
[Crossref] [PubMed]

Zhou, Q.

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

Zhu, B.

P. Huang, X. Xu, L. Wang, B. Zhu, X. Wang, and J. Xia, “The role of EGF-EGFR signalling pathway in hepatocellular carcinoma inflammatory microenvironment,” J. Cell. Mol. Med. 18(2), 218–230 (2014).
[Crossref] [PubMed]

Ziebart, A.

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

Adv. Drug Deliv. Rev. (1)

G. M. Thurber, M. M. Schmidt, and K. D. Wittrup, “Antibody tumor penetration: transport opposed by systemic and antigen-mediated clearance,” Adv. Drug Deliv. Rev. 60(12), 1421–1434 (2008).
[Crossref] [PubMed]

Am. J. Clin. Pathol. (1)

A. F. Buckley, L. J. Burgart, V. Sahai, and S. Kakar, “Epidermal growth factor receptor expression and gene copy number in conventional hepatocellular carcinoma,” Am. J. Clin. Pathol. 129(2), 245–251 (2008).
[Crossref] [PubMed]

Asian J. Endosc. Surg. (1)

T. Ishizawa, Y. Bandai, N. Harada, A. Muraoka, M. Ijichi, K. Kusaka, M. Shibasaki, and N. Kokudo, “Indocyanine green-fluorescent imaging of hepatocellular carcinoma during laparoscopic hepatectomy: An initial experience,” Asian J. Endosc. Surg. 3(1), 42–45 (2010).
[Crossref]

Biomed. Instrum. Technol. (1)

Y. Chen, X. Intes, and B. Chance, “Development of high-sensitivity near-infrared fluorescence imaging device for early cancer detection,” Biomed. Instrum. Technol. 39(1), 75–85 (2005).
[PubMed]

Chem. Rev. (1)

S. Lee, J. Xie, and X. Chen, “Peptides and peptide hormones for molecular imaging and disease diagnosis,” Chem. Rev. 110(5), 3087–3111 (2010).
[Crossref] [PubMed]

Clin. Transl. Gastroenterol. (1)

J. Zhou, B. P. Joshi, X. Duan, A. Pant, Z. Qiu, R. Kuick, S. R. Owens, and T. D. Wang, “EGFR Overexpressed in Colonic Neoplasia Can be Detected on Wide-Field Endoscopic Imaging,” Clin. Transl. Gastroenterol. 6(7), e101 (2015).
[Crossref] [PubMed]

Eur. J. Surg. Oncol. (1)

T. Abo, A. Nanashima, S. Tobinaga, S. Hidaka, N. Taura, K. Takagi, J. Arai, H. Miyaaki, H. Shibata, and T. Nagayasu, “Usefulness of intraoperative diagnosis of hepatic tumors located at the liver surface and hepatic segmental visualization using indocyanine green-photodynamic eye imaging,” Eur. J. Surg. Oncol. 41(2), 257–264 (2015).
[Crossref] [PubMed]

Gastroenterology (1)

M. Goetz, A. Ziebart, S. Foersch, M. Vieth, M. J. Waldner, P. Delaney, P. R. Galle, M. F. Neurath, and R. Kiesslich, “In vivo molecular imaging of colorectal cancer with confocal endomicroscopy by targeting epidermal growth factor receptor,” Gastroenterology 138(2), 435–446 (2010).
[Crossref] [PubMed]

J. Cell. Mol. Med. (1)

P. Huang, X. Xu, L. Wang, B. Zhu, X. Wang, and J. Xia, “The role of EGF-EGFR signalling pathway in hepatocellular carcinoma inflammatory microenvironment,” J. Cell. Mol. Med. 18(2), 218–230 (2014).
[Crossref] [PubMed]

J. Visc. Surg. (1)

C. Lim, E. Vibert, D. Azoulay, C. Salloum, T. Ishizawa, R. Yoshioka, Y. Mise, Y. Sakamoto, T. Aoki, Y. Sugawara, K. Hasegawa, and N. Kokudo, “Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications,” J. Visc. Surg. 151(2), 117–124 (2014).
[Crossref] [PubMed]

Oncologist (1)

A. P. Venook, C. Papandreou, J. Furuse, and L. L. de Guevara, “The incidence and epidemiology of hepatocellular carcinoma: a global and regional perspective,” Oncologist 15(Suppl 4), 5–13 (2010).
[Crossref] [PubMed]

Photoacoustics (1)

Q. Zhou, Z. Li, J. Zhou, B. P. Joshi, G. Li, X. Duan, R. Kuick, S. R. Owens, and T. D. Wang, “In Vivo Photoacoustic Tomography of EGFR Overexpressed in Hepatocellular Carcinoma Mouse Xenograft,” Photoacoustics 4, 1–12 (2016).
[PubMed]

Semin. Liver Dis. (1)

J. M. Llovet, M. Schwartz, and V. Mazzaferro, “Resection and liver transplantation for hepatocellular carcinoma,” Semin. Liver Dis. 25(2), 181–200 (2005).
[Crossref] [PubMed]

Surg. Endosc. (1)

I. Dagher, P. Lainas, A. Carloni, C. Caillard, A. Champault, C. Smadja, and D. Franco, “Laparoscopic liver resection for hepatocellular carcinoma,” Surg. Endosc. 22(2), 372–378 (2008).
[Crossref] [PubMed]

Other (1)

Venugopal V, Park M, Ashitate Y, Neacsu F, Kettenring F, Frangioni JV, Gangadharan SP, Gioux S. Design and characterization of an optimized simultaneous color and near-infrared fluorescence rigid endoscopic imaging system. J Biomed Opt 2013;18:126018.1.

Supplementary Material (3)

NameDescription
» Visualization 1: MP4 (523 KB)      visualization1
» Visualization 2: MP4 (1042 KB)      visualization2
» Visualization 3: MP4 (587 KB)      visualization3

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Figures (5)

Fig. 1
Fig. 1 Schematic. Light leaving proximal end of laparoscope is split by dichroic mirror (DM). Reflectance at λex = 660 nm is attenuated by neutral density filter (ND) and focused by objective O1 onto color camera CCD1. NIR fluorescence is bandpass filtered (BPF) at center wavelength λ = 716 nm over a 40 nm band and is focused by objective O2 onto monochrome camera CCD2.

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Fig. 2
Fig. 2 NIR fluorescence laparoscope. A compact imaging module that contains the optics, filters, and cameras shown in Fig. 1 is attached to the proximal end of a standard laparoscope. Fluorescence excitation at λex = 660 nm is delivered through a fiber optic light guide attached to a side port.

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Fig. 3
Fig. 3 Pharmacokinetics of EGFR peptide in HCC xenograft. The target-to-background (T/B) ratio for 13 HCC xenograft tumors in 5 mice was measured over time following injection of either QRH*-Cy5.5 or PEH*-Cy5.5. For QRH*-Cy5.5, the T/B ratio reached a maximum value of 2.53 ± 0.20 at 6 hours. For PEH*-Cy5.5, the T/B ratio was significantly less at each time point, *P < 0.01 by unpaired t-test.

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Fig. 4
Fig. 4 In vivo images of HCC xenograft tumors. Representative a) white light, b) reflectance, and c) fluorescence images were collected with the NIR laparoscope ∼6 hours after intravenous injection of the EGFR peptide QRH*-Cy5.5 are shown. d-f) The same set of images were collected with scrambled peptide PEH*-Cy5.5 in a different tumor.

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Fig. 5
Fig. 5 EGFR peptide binding to xenograft tumors. a) We quantified T/B ratios from in vivo images collected from 13 tumors in 5 mice for either QRH*-Cy5.5 or PEH*-Cy5.5 and found mean ± std of 2.99 ± 0.22 versus 1.81 ± 0.16, respectively, P < 0.0001 by unpaired t-test. Representative confocal fluorescence microscopy of excised tumor sections are shown for b) QRH*-Cy5.5 and c) PEH*-Cy5.5 at 63X magnification. Note intense staining of QRH*-Cy5.5 to surface of SK-Hep1 human HCC cells.

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