Surgical Endoscopy

, Volume 31, Issue 12, pp 5111–5118 | Cite as

Applications of fusion-fluorescence imaging using indocyanine green in laparoscopic hepatectomy

  • Muga Terasawa
  • Takeaki IshizawaEmail author
  • Yoshihiro Mise
  • Yosuke Inoue
  • Hiromichi Ito
  • Yu Takahashi
  • Akio Saiura



Indocyanine green (ICG)-fluorescence imaging has been developed for real-time identification of hepatic tumors and segmental boundaries during hepatectomy. Fusion ICG-fluorescence imaging (real-time visualization of pseudocolor-fluorescence signals on white-light color images) may serve as a reliable navigation tool especially in laparoscopic hepatectomy, in which gross inspection and palpation are limited.


The study population consisted of 41 patients undergoing laparoscopic hepatectomy. Hepatic tumors were identified by fluorescence imaging following the preoperative intravenous administration of ICG (0.5 mg/kg body weight). To visualize hepatic perfusion and segmental boundaries, ICG (1.25 mg) was injected intravenously during surgery, following closure of the proximal portal pedicle. A laparoscopic imaging system, which enabled superimposition of the pseudocolor-fluorescence images on white color images, was used for the fusion ICG-fluorescence imaging.


Among the 53 malignant tumors resected, fusion ICG-fluorescence imaging revealed 45 nodules (85%), including three nodules of colorectal liver metastasis unidentifiable by white-light color images or intraoperative ultrasonography. It also delineated the segmental boundaries on the hepatic raw surfaces as well as on the phrenic/visceral surfaces in all 12 patients evaluated using this technique.


Fusion imaging enhances the feasibility of intraoperative ICG-fluorescence imaging in the identification of hepatic tumors and segmental boundaries. It may therefore help surgeons in the safe and accurate completion of laparoscopic hepatectomies.


Laparoscopic hepatectomy Indocyanine green Fluorescence imaging Hepatic segmentectomy Colorectal liver metastasis 



This work was supported by Grants from the Mochida Memorial Foundation for Medical, Foundation for Promotion of Cancer Research in Japan and Pharmaceutical Research and the Japan Agency for Medical Research and Development.

Compliance with ethical standards


Drs. Takeaki Ishizawa, Yosuke Inoue, Yoshihiro Mise, Yu Takahashi, and Akio Saiura have no conflicts of interest or financial ties to disclose.

Supplementary material

Video, Supplemental Digital Content 1. Laparoscopic hepatectomy of S4sup extended to S3 and S4inf based on the ICG-fluorescence images. Supplementary material 1 (WMV 10902 kb)

Video, Supplemental Digital Content 2. ICG-fluorescence imaging identifies small colorectal metastases, located in S3 and S6, after preoperative chemotherapy. Supplementary material 2 (WMV 10289 kb)

Video, Supplemental Digital Content 3. Visualization of the segmental boundaries by fluorescence imaging after the intraoperative intravenous injection of ICG; hepatic resection of S5 was extended to include S6. Supplementary material 3 (WMV 10640 kb)

Video, Supplemental Digital Content 4. Visualization of the segmental boundaries by fluorescence imaging after the intraoperative intravenous injection of ICG; a limited resection of S3 with small extension to S2 was performed. Supplementary material 4 (WMV 10425 kb)


  1. 1.
    Dip FD, Ishizawa T, Kokudo N, Rosenthal R (eds) (2015) Fluorescence imaging for surgeons. Springer International Publishing, Switzerland, ChamGoogle Scholar
  2. 2.
    Rosenthal EL, Warram JM, de Boer E, Basilion JP, Biel MA, Bogyo M, Bouvet M, Brigman BE, Colson YL, DeMeester SR, Gurtner GC, Ishizawa T, Jacobs PM, Keereweer S, Liao JC, Nguyen QT, Olson JM, Paulsen KD, Rieves D, Sumer BD, Tweedle MF, Vahrmeijer AL, Weichert JP, Wilson BC, Zenn MR, Zinn KR, van Dam GM (2016) Successful translation of fluorescence navigation during oncologic surgery: a consensus report. J Nucl Med 57(1):144–150CrossRefPubMedGoogle Scholar
  3. 3.
    Reuthebuch O, Haussler A, Genoni M, Tavakoli R, Odavic D, Kadner A, Turina M (2004) Novadaq SPY: intraoperative quality assessment in off-pump coronary artery bypass grafting. Chest 125:418–424CrossRefPubMedGoogle Scholar
  4. 4.
    Kitai T, Inomoto T, Miwa M, Shikayama T (2005) Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer 12:211–215CrossRefPubMedGoogle Scholar
  5. 5.
    Ishizawa T, Tamura S, Masuda K, Aoki T, Hasegawa K, Imamura H, Beck Y, Kokudo N (2008) Intraoperative fluorescent cholangiography using indocyanine green: a biliary road map for safe surgery. J Am Coll Surg 208:e1–e4CrossRefPubMedGoogle Scholar
  6. 6.
    Mitsuhashi N, Kimura F, Shimizu H, Imamaki M, Yoshidome H, Ohtsuka M, Kato A, Yoshitomi H, Nozawa S, Furukawa K, Takeuchi D, Takayashiki T, Suda K, Igarashi T, Miyazaki M (2008) Usefulness of intraoperative fluorescence imaging to evaluate local anatomy in hepatobiliary surgery. J Hepatobiliary Pancreat Surg 15:508–514CrossRefPubMedGoogle Scholar
  7. 7.
    Ishizawa T, Bandai Y, Kokudo N (2009) Fluorescent cholangiography using indocyanine green for laparoscopic cholecystectomy: an initial experience. Arch Surg 144:381–382CrossRefPubMedGoogle Scholar
  8. 8.
    Ishizawa T, Bandai Y, Ijichi M, Kokudo N (2010) Fluorescent cholangiography illuminating the biliary tree during laparoscopic cholecystectomy. Br J Surg 97:1369–1377CrossRefPubMedGoogle Scholar
  9. 9.
    Ishizawa T, Fukushima N, Shibahara J, Masuda K, Tamura S, Aoki T, Hasegawa K, Beck Y, Fukayama M, Kokudo N (2009) Real-time identification of liver cancers by using indocyanine green fluorescent imaging. Cancer 115:2491–2504CrossRefPubMedGoogle Scholar
  10. 10.
    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 100:75–79CrossRefPubMedGoogle Scholar
  11. 11.
    Yokoyama N, Otani T, Hashidate H, Maeda C, Katada T, Sudo N, Manabe S, Ikeno Y, Toyoda A, Katayanagi N (2012) Real-time detection of hepatic micrometastases from pancreatic cancer by intraoperative fluorescence imaging: Preliminary results of a prospective study. Cancer 118:2813–2819CrossRefPubMedGoogle Scholar
  12. 12.
    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):3411–3418CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Ishizawa T, Masuda K, Urano Y, Kawaguchi Y, Satou S, Kaneko J, Hasegawa K, Shibahara J, Fukayama M, Tsuji S, Midorikawa Y, Aburatani H, Kokudo N (2014) Mechanistic background and clinical applications of indocyanine green-fluorescence imaging of hepatocellular carcinoma. Ann Surg Oncol 21:440–448CrossRefPubMedGoogle Scholar
  14. 14.
    Aoki T, Yasuda D, Shimizu Y, Odaira M, Niiya T, Kusano T, Mitamura K, Hayashi K, Murai N, Koizumi T, Kato H, Enami Y, Miwa M, Kusano M (2008) Image-guided liver mapping using fluorescence navigation system with indocyanine green for anatomical hepatic resection. World J Surg 32:1763–1767CrossRefPubMedGoogle Scholar
  15. 15.
    Ishizawa T, Zuker NB, Kokudo N, Gayet B (2012) Positive and negative staining of hepatic segments by use of fluorescent imaging techniques during laparoscopic hepatectomy. Arch Surg 147:393–394CrossRefPubMedGoogle Scholar
  16. 16.
    Inoue Y, Arita J, Sakamoto T, Ono Y, Takahashi M, Takahashi Y, Kokudo N, Saiura A (2015) Anatomical liver resections guided by 3-dimensional parenchymal staining using fusion indocyanine green fluorescence imaging. Ann Surg 262(1):105–111CrossRefPubMedGoogle Scholar
  17. 17.
    Miyata A, Ishizawa T, Tani K, Shimizu A, Kaneko J, Aoki T, Sakamoto Y, Sugawara Y, Hasegawa K, Kokudo N (2015) Reappraisal of a dye-staining technique for anatomic hepatectomy by the concomitant use of indocyanine green fluorescence imaging. J Am Coll Surg Aug 221:e27–e36Google Scholar
  18. 18.
    Landsman ML, Kwant G, Mook GA, Zijlstra WG (1976) Light-absorbing properties, stability, and spectral stabilization of indocyanine green. J Appl Physiol 40:575–583PubMedGoogle Scholar
  19. 19.
    Cherrick GR, Stein SW, Leevy CM, Davidson CS (1960) Indocyanine green: observations on its physical properties, plasma decay, and hepatic extraction. J Clin Invest 39:592–600CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Spinoglio G, Priora F, Bianchi PP, Lucido FS, Licciardello A, Maglione V, Grosso F, Quarati R, Ravazzoni F, Lenti LM (2013) Real-time near-infrared (NIR) fluorescent cholangiography in single-site robotic cholecystectomy (SSRC): a single-institutional prospective study. Surg Endosc 27:2156–2162CrossRefPubMedGoogle Scholar
  21. 21.
    Kudo H, Ishizawa T, Tani K, Harada N, Ichida A, Shimizu A, Kaneko J, Aoki T, Sakamoto Y, Sugawara Y, Hasegawa K, Kokudo N (2014) Visualization of subcapsular hepatic malignancy by indocyanine-green fluorescence imaging during laparoscopic hepatectomy. Surg Endosc 28:2504–2508CrossRefPubMedGoogle Scholar
  22. 22.
    Kono Y, Ishizawa T, Tani K, Harada N, Kaneko J, Saiura A, Bandai Y, Kokudo N (2015) Techniques of fluorescence cholangiography during laparoscopic cholecystectomy for better delineation of the bile duct anatomy. Medicine (Baltimore) 94:e1005CrossRefGoogle Scholar
  23. 23.
    Arita J, Takahashi M, Hata S, Shindoh J, Beck Y, Sugawara Y, Hasegawa K, Kokudo N (2011) Usefulness of contrast-enhanced intraoperative ultrasound using Sonazoid in patients with hepatocellular carcinoma. Ann Surg 254(6):992–999CrossRefPubMedGoogle Scholar
  24. 24.
    Takahashi M, Hasegawa K, Arita J, Hata S, Aoki T, Sakamoto Y, Sugawara Y, Kokudo N (2012) Contrast-enhanced intraoperative ultrasonography using perfluorobutane microbubbles for the enumeration of colorectal liver metastases. Br J Surg 99(9):1271–1277CrossRefPubMedGoogle Scholar
  25. 25.
    Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, Asbun H, OʼRourke N, Tanabe M, Koffron AJ, Tsung A, Soubrane O, Machado MA, Gayet B, Troisi RI, Pessaux P, Van Dam RM, Scatton O, Abu Hilal M, Belli G, Kwon CH, Edwin B, Choi GH, Aldrighetti LA, Cai X, Cleary S, Chen KH, Schön MR, Sugioka A, Tang CN, Herman P, Pekolj J, Chen XP, Dagher I, Jarnagin W, Yamamoto M, Strong R, Jagannath P, Lo CM, Clavien PA, Kokudo N, Barkun J, Strasberg SM (2015) Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 261(4):619–629Google Scholar
  26. 26.
    Ishizawa T, Gumbs AA, Kokudo N, Gayet B (2012) Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 256:959–964CrossRefPubMedGoogle Scholar
  27. 27.
    Kawaguchi Y, Velayutham V, Fuks D, Christidis C, Kokudo N, Gayet B (2015) Usefulness of indocyanine green-fluorescence imaging for visualization of the bile duct during laparoscopic liver resection. J Am Coll Surg 221(6):e113–e117CrossRefPubMedGoogle Scholar
  28. 28.
    Kaibori M, Ishizaki M, Matsui K, Kwon AH (2011) Intraoperative indocyanine green fluorescent imaging for prevention of bile leakage after hepatic resection. Surgery 150(1):91–98CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Department of Gastroenterological Surgery, Cancer Institute HospitalJapanese Foundation for Cancer ResearchTokyoJapan

Personalised recommendations