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Published in: Journal of Cancer Research and Clinical Oncology 1/2017

Open Access 01-01-2017 | Original Article – Cancer Research

Liver tumor boundaries identified intraoperatively using real-time indocyanine green fluorescence imaging

Authors: Ya-Min Zhang, Rui Shi, Jian-Cun Hou, Zi-Rong Liu, Zi-Lin Cui, Yang Li, Di Wu, Yuan Shi, Zhong-Yang Shen

Published in: Journal of Cancer Research and Clinical Oncology | Issue 1/2017

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Abstract

Purpose

Clear delineation between tumors and normal tissues is ideal for real-time surgical navigation imaging. We investigated applying indocyanine green (ICG) fluorescence imaging navigation using an intraoperative administration method in liver resection.

Methods

Fifty patients who underwent liver resection were divided into two groups based on clinical situation and operative purpose. In group I, sizes of superficial liver tumors were determined; tiny tumors were identified. In group II, the liver resection margin was determined; real-time navigation was performed. ICG was injected intravenously at the beginning of the operation; the liver surface was observed with a photodynamic eye (PDE).

Results

Liver resection margins were determined using PDE. Fluorescence contrast between normal liver and tumor tissues was obvious in 32 of 35 patients. A boundary for half the liver or specific liver segments was determined in nine patients by examining the portal vein anatomy after ICG injection. Eight small tumors not observed preoperatively were detected; the smallest was 2 mm.

Conclusions

ICG fluorescence imaging navigation is a promising, simple, and safe tool for routine real-time intraoperative imaging during hepatic resection and clinical exploration in hepatocellular carcinoma, enabling high sensibility for identifying liver resection margins and detecting tiny superficial tumors.
Literature
go back to reference Abo T, Nanashima A, Tobinaga S, Hidaka S, Taura N, Takagi K, Arai J, Miyaaki H, Shibata H, Nagayasu T (2015) 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):257–264CrossRefPubMed Abo T, Nanashima A, Tobinaga S, Hidaka S, Taura N, Takagi K, Arai J, Miyaaki H, Shibata H, Nagayasu T (2015) 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):257–264CrossRefPubMed
go back to reference Adusumilli PS, Stiles BM, Chan MK, Eisenberg DP, Yu Z, Stanziale SF, Huq R, Wong RJ, Rusch VW, Fong Y (2006) Real-time diagnostic imaging of tumors and metastases by use of a replication-competent herpes vector to facilitate minimally invasive oncological surgery. FASEB J 20:726–728PubMedPubMedCentral Adusumilli PS, Stiles BM, Chan MK, Eisenberg DP, Yu Z, Stanziale SF, Huq R, Wong RJ, Rusch VW, Fong Y (2006) Real-time diagnostic imaging of tumors and metastases by use of a replication-competent herpes vector to facilitate minimally invasive oncological surgery. FASEB J 20:726–728PubMedPubMedCentral
go back to reference de Chermont QLM, Chaneac C, Seguin J, Pellé F, Maîtrejean S, Jolivet JP, Gourier D, Bessodes M, Scherman D (2007) Nanoprobes with near-infrared persistent luminescence for in vivo imaging. Proc Natl Acad Sci USA 104:9266–9271CrossRef de Chermont QLM, Chaneac C, Seguin J, Pellé F, Maîtrejean S, Jolivet JP, Gourier D, Bessodes M, Scherman D (2007) Nanoprobes with near-infrared persistent luminescence for in vivo imaging. Proc Natl Acad Sci USA 104:9266–9271CrossRef
go back to reference de Graaf W, Häusler S, Heger M, van Ginhoven TM, van Cappellen G, Bennink RJ, Kullak-Ublick GA, Hesselmann R, van Gulik TM, Stieger B (2011) Transporters involved in the hepatic uptake of (99 m)Tc-mebrofenin and indocyanine green. J Hepatol 54(4):738–745CrossRefPubMed de Graaf W, Häusler S, Heger M, van Ginhoven TM, van Cappellen G, Bennink RJ, Kullak-Ublick GA, Hesselmann R, van Gulik TM, Stieger B (2011) Transporters involved in the hepatic uptake of (99 m)Tc-mebrofenin and indocyanine green. J Hepatol 54(4):738–745CrossRefPubMed
go back to reference Gotoh K, Yamada T, Ishikawa O, Takahashi H, Eguchi H, Yano M, Ohigashi H, Tomita Y, Miyamoto Y, Imaoka S (2009) A novel image-guided surgery of hepatocellular carcinoma by indocyanine green fluorescence imaging navigation. J Surg Oncol 100(1):75–79CrossRefPubMed Gotoh K, Yamada T, Ishikawa O, Takahashi H, Eguchi H, Yano M, Ohigashi H, Tomita Y, Miyamoto Y, Imaoka S (2009) A novel image-guided surgery of hepatocellular carcinoma by indocyanine green fluorescence imaging navigation. J Surg Oncol 100(1):75–79CrossRefPubMed
go back to reference Ishizawa T, Kokudo N (2013) Identification of hepatocellular carcinoma. Fluoresc Imaging 31:10–17CrossRef Ishizawa T, Kokudo N (2013) Identification of hepatocellular carcinoma. Fluoresc Imaging 31:10–17CrossRef
go back to reference Ishizawa T, Zuker NB, Kokudo N, Gayet B (2012) Positive and negative staining of hepatic segments by use of fluorescent imaging techniques during laparoseopichepateetomy. Arch Surg 147(4):393–394CrossRefPubMed Ishizawa T, Zuker NB, Kokudo N, Gayet B (2012) Positive and negative staining of hepatic segments by use of fluorescent imaging techniques during laparoseopichepateetomy. Arch Surg 147(4):393–394CrossRefPubMed
go back to reference Kawaguchi Y, Aoki T, Ishizawa T, Arita J, Satou S, Kaneko J, Sakamoto Y, Sugawara Y, Hasegawa K, Kokudo N (2013) Education and imaging: hepatobiliary and pancreatic: identification of recurrent hepatocellular carcinoma by intraoperative fluorescent imaging. J Gastroenterol Hepatol 28(3):587CrossRefPubMed Kawaguchi Y, Aoki T, Ishizawa T, Arita J, Satou S, Kaneko J, Sakamoto Y, Sugawara Y, Hasegawa K, Kokudo N (2013) Education and imaging: hepatobiliary and pancreatic: identification of recurrent hepatocellular carcinoma by intraoperative fluorescent imaging. J Gastroenterol Hepatol 28(3):587CrossRefPubMed
go back to reference Kitai T, Miwa M, Liu H, Beauvoit B, Chance B, Yamaoka Y (1999) Application of near-infrared time resolved spectroscopy to rat liver—a preliminary report for surgical application. Phys Med Biol 44:2049–2061CrossRefPubMed Kitai T, Miwa M, Liu H, Beauvoit B, Chance B, Yamaoka Y (1999) Application of near-infrared time resolved spectroscopy to rat liver—a preliminary report for surgical application. Phys Med Biol 44:2049–2061CrossRefPubMed
go back to reference Kitai T, Inomoto T, Miwa M, Shikayama T (2005) Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer 12:211–215CrossRefPubMed Kitai T, Inomoto T, Miwa M, Shikayama T (2005) Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer 12:211–215CrossRefPubMed
go back to reference Kurihara T, Yamashita Y, Yoshida Y, Takeishi K, Itoh S, Harimoto N, Yoshizumi T, Shirabe K, Ikeda T, Maehara Y (2015) Indocyanine green fluorescent imaging for hepatic resection of the right hepatic vein drainage area. J Am Coll Surg 221(3):e49–e53CrossRefPubMed Kurihara T, Yamashita Y, Yoshida Y, Takeishi K, Itoh S, Harimoto N, Yoshizumi T, Shirabe K, Ikeda T, Maehara Y (2015) Indocyanine green fluorescent imaging for hepatic resection of the right hepatic vein drainage area. J Am Coll Surg 221(3):e49–e53CrossRefPubMed
go back to reference Lim C, Vibert E (2013) Identification of metastatic liver cancer. Fluoresc Imaging 31:18–24CrossRef Lim C, Vibert E (2013) Identification of metastatic liver cancer. Fluoresc Imaging 31:18–24CrossRef
go back to reference Lim C, Vibert E, Azoulay D, Salloum C, Ishizawa T, Yoshioka R, Mise Y, Sakamoto Y, Aoki T, Sugawara Y et al (2014) Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications. J Visc Surg 151(2):117–124CrossRefPubMed Lim C, Vibert E, Azoulay D, Salloum C, Ishizawa T, Yoshioka R, Mise Y, Sakamoto Y, Aoki T, Sugawara Y et al (2014) Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications. J Visc Surg 151(2):117–124CrossRefPubMed
go back to reference Miyashiro I, Miyoshi N, Hiratsuka M, Kishi K, Yamada T, Ohue M, Ohigashi H, Yano M, Ishikawa O, Imaoka S (2008) Detection of sentinel node in gastric cancer surgery by indocyanine green fluorescence imaging: comparison with infrared imaging. Ann Surg Oncol 15:1640–1643CrossRefPubMed Miyashiro I, Miyoshi N, Hiratsuka M, Kishi K, Yamada T, Ohue M, Ohigashi H, Yano M, Ishikawa O, Imaoka S (2008) Detection of sentinel node in gastric cancer surgery by indocyanine green fluorescence imaging: comparison with infrared imaging. Ann Surg Oncol 15:1640–1643CrossRefPubMed
go back to reference Morise Z, Kawabe N, Tomishige H, Nagata H, Kawase J, Arakawa S, Yoshida R, Isetani M (2014) Recent advances in liver resection for hepatocellular carcinoma. Front Surg 1(21):1–8 Morise Z, Kawabe N, Tomishige H, Nagata H, Kawase J, Arakawa S, Yoshida R, Isetani M (2014) Recent advances in liver resection for hepatocellular carcinoma. Front Surg 1(21):1–8
go back to reference Morita Y, Sakaguchi T, Unno N, Shibasaki Y, Suzuki A, Fukumoto K, Inaba K, Baba S, Takehara Y, Suzuki S, Konno H (2013) Detection of hepatocellular carcinomas with near-infrared fluorescence imaging using indocyanine green: its usefulness and limitation. Int J Oncol 18:232–241CrossRef Morita Y, Sakaguchi T, Unno N, Shibasaki Y, Suzuki A, Fukumoto K, Inaba K, Baba S, Takehara Y, Suzuki S, Konno H (2013) Detection of hepatocellular carcinomas with near-infrared fluorescence imaging using indocyanine green: its usefulness and limitation. Int J Oncol 18:232–241CrossRef
go back to reference Porcu EP, Salis A, Gavini E, Rassu G, Maestri M, Giunchedi P (2016) Indocyanine green delivery systems for tumour detection and treatments. Biotechnol Adv 34(5):768–789CrossRefPubMed Porcu EP, Salis A, Gavini E, Rassu G, Maestri M, Giunchedi P (2016) Indocyanine green delivery systems for tumour detection and treatments. Biotechnol Adv 34(5):768–789CrossRefPubMed
go back to reference Shibasaki Y, Sakaguchi T, Hiraide T, Morita Y, Suzuki A, Baba S, Setou M, Konno H (2015) Expression of indocyanine green-related transporters in hepatocellular carcinoma. J Surg Res 193(2):567–576CrossRefPubMed Shibasaki Y, Sakaguchi T, Hiraide T, Morita Y, Suzuki A, Baba S, Setou M, Konno H (2015) Expression of indocyanine green-related transporters in hepatocellular carcinoma. J Surg Res 193(2):567–576CrossRefPubMed
go back to reference Tsujino Y, Mizumoto K, Matsuzaka Y, Niihara H, Morita E (2009) Fluorescence navigation with indocyanine green for detecting sentinel nodes in extramammary Paget’s disease and squamous cell carcinoma. J Dermatol 36:90–94CrossRefPubMed Tsujino Y, Mizumoto K, Matsuzaka Y, Niihara H, Morita E (2009) Fluorescence navigation with indocyanine green for detecting sentinel nodes in extramammary Paget’s disease and squamous cell carcinoma. J Dermatol 36:90–94CrossRefPubMed
go back to reference van der Vorst JR, Hutteman M, Mieog JS, de Rooij KE, Kaijzel EL, Löwik CW, Putter H, Kuppen PJ, Frangioni JV, van de Velde CJ, Vahrmeijer AL (2012) Near-infrared fluorescence imaging of liver metastases in rats using indocyanine green. J Surg Res 174(2):266–271CrossRefPubMed van der Vorst JR, Hutteman M, Mieog JS, de Rooij KE, Kaijzel EL, Löwik CW, Putter H, Kuppen PJ, Frangioni JV, van de Velde CJ, Vahrmeijer AL (2012) Near-infrared fluorescence imaging of liver metastases in rats using indocyanine green. J Surg Res 174(2):266–271CrossRefPubMed
go back to reference van der Vorst JR, Schaafsma BE, Hutteman M, Verbeek FP, Liefers GJ, Hartgrink HH, Smit VT, Löwik CW, van de Velde CJ, Frangioni JV, Vahrmeijer AL (2013) Near infrared fluorescence guided resection of colorectal liver metastases. Cancer 119(18):3411–3418CrossRefPubMedPubMedCentral van der Vorst JR, Schaafsma BE, Hutteman M, Verbeek FP, Liefers GJ, Hartgrink HH, Smit VT, Löwik CW, van de Velde CJ, Frangioni JV, Vahrmeijer AL (2013) Near infrared fluorescence guided resection of colorectal liver metastases. Cancer 119(18):3411–3418CrossRefPubMedPubMedCentral
go back to reference Veiseh M, Gabikian P, Bahrami SB, Veiseh O, Zhang M, Hackman RC, Ravanpay AC, Stroud MR, Kusuma Y, Hansen SJ et al (2007) Tumor paint: a chlorotoxin:Cy5.5 bioconjugate for intraoperative visualization of cancer foci. Cancer Res 67:6882–6888CrossRefPubMed Veiseh M, Gabikian P, Bahrami SB, Veiseh O, Zhang M, Hackman RC, Ravanpay AC, Stroud MR, Kusuma Y, Hansen SJ et al (2007) Tumor paint: a chlorotoxin:Cy5.5 bioconjugate for intraoperative visualization of cancer foci. Cancer Res 67:6882–6888CrossRefPubMed
go back to reference Verbeek FP, van der Vorst JR, Schaafsma BE et al (2012) Image-guided cancer surgery: the value of near-infrared fluorescence imaging during oncologic and gastrointestinal procedures. J Hepatobiliary Pancreat Sci 19(6):626–637CrossRefPubMedPubMedCentral Verbeek FP, van der Vorst JR, Schaafsma BE et al (2012) Image-guided cancer surgery: the value of near-infrared fluorescence imaging during oncologic and gastrointestinal procedures. J Hepatobiliary Pancreat Sci 19(6):626–637CrossRefPubMedPubMedCentral
Metadata
Title
Liver tumor boundaries identified intraoperatively using real-time indocyanine green fluorescence imaging
Authors
Ya-Min Zhang
Rui Shi
Jian-Cun Hou
Zi-Rong Liu
Zi-Lin Cui
Yang Li
Di Wu
Yuan Shi
Zhong-Yang Shen
Publication date
01-01-2017
Publisher
Springer Berlin Heidelberg
Published in
Journal of Cancer Research and Clinical Oncology / Issue 1/2017
Print ISSN: 0171-5216
Electronic ISSN: 1432-1335
DOI
https://doi.org/10.1007/s00432-016-2267-4

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