The clinical application and progress of indocyanine green-fluorescence imaging in liver tumor surgery_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

HE Pan ¹ , FANG Cheng ¹ , SU Song ¹ , HE Kai ¹ , GAN Yu ¹ , TIAN Jie ² , LI Bo ¹ ,  XIA Xianming ¹

1. Deportment of Hepatobiliary Surgery, Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan 646000, P. R. China;
2. Key Laboratory of Molecular Imaging of Chinese Academy of Sciences, Institute of Automation, Chinese Academy of Sciences, Beijing 100190, P. R. China;

Corresponding author：

XIA Xianming, Email: xxm6206@126.com

Keywords：

indocyanine green; fluorescence imaging; liver tumor; clinical application; review

DOI：

10.7507/1007-9424.201801005

Video：

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Objective To summarize the application and progress of the indocyanine green-fluorescence imaging in liver tumor surgery, at the same time, to demonstrate the advantages, limitations, and prospects of this technology. Methods Clinical researches about indocyanine green-fluorescence imaging in liver tumor surgery were collected, to review the introduction and principle of indocyanine green-fluorescence imaginging, and its clinical application of detecting small lesions and demarcating boundaries in liver tumor surgery. Results Indocyanine green-fluorescence imaging had been used in liver tumors surgery. In the aspect of locating the tumors, detecting small lesions, and demarcating boundaries, it had begun to show its unique value. And it was provided to be a new way to reduce tumor recurrence, improve treatment effect, and prolong survival time. Conclusions Indocyanine green-fluorescence imaging is now in the stage of development and promotion, and it has great development potential in technology. But, it also needs advancement in identification ability of benign and malignant lesions, and the depth of detection.

Citation： HE Pan, FANG Cheng, SU Song, HE Kai, GAN Yu, TIAN Jie, LI Bo, XIA Xianming. The clinical application and progress of indocyanine green-fluorescence imaging in liver tumor surgery. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2018, 25(8): 1011-1015. doi: 10.7507/1007-9424.201801005 Copy

1.	Llovet JM, Bruix J. Novel advancements in the management of hepatocellular carcinoma in 2008. J Hepatol, 2008, 48 Suppl 1: S20-S37.
2.	Ishizawa T, Fukushima N, Shibahara J, et al. Real-time identification of liver cancers by using indocyanine green fluorescent imaging. Cancer, 2009, 115(11): 2491-2504.
3.	Herschman HR. Molecular imaging: looking at problems, seeing solutions. Science, 2003, 302(5645): 605-608.
4.	Jaffer FA, Weissleder R. Molecular imaging in the clinical arena. JAMA, 2005, 293(7): 855-862.
5.	Benson RC, Kues HA. Fluorescence properties of indocyanine green as related to angiography. Phys Med Biol, 1978, 23(1): 159-163.
6.	Morton CA, Brown SB, Collins S, et al. Guidelines for topical photodynamic therapy: report of a workshop of the British Photodermatology Group. Br J Dermatol, 2002, 146(4): 552-567.
7.	Stummer W, Stocker S, Wagner S, et al. Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery, 1998, 42(3): 518-525.
8.	Unno N, Inuzuka K, Suzuki M, et al. Preliminary experience with a novel fluorescence lymphography using indocyanine green in patients with secondary lymphedema. J Vasc Surg, 2007, 45(5): 1016-1021.
9.	Unno N, Suzuki M, Yamamoto N, et al. Indocyanine green fluorescence angiography for intraoperative assessment of blood flow: a feasibility study. Eur J Vasc Endovasc Surg, 2008, 35(2): 205-207.
10.	Lam B, Wong MP, Fung SL, et al. The clinical value of autofluorescence bronchoscopy for the diagnosis of lung cancer. Eur Respir J, 2006, 28(5): 915-919.
11.	Kusano M, Tajima Y, Yamazaki K, et al. Sentinel node mapping guided by indocyanine green fluorescence imaging: a new method for sentinel node navigation surgery in gastrointestinal cancer. Dig Surg, 2008, 25(2): 103-108.
12.	Ishizawa T, Tamura S, Masuda K, et al. Intraoperative fluorescent cholangiography using indocyanine green: a biliary road map for safe surgery. J Am Coll Surg, 2009, 208(1): e1-e4.
13.	Ishizawa T, Bandai Y, Ijichi M, et al. Fluorescent cholangiography illuminating the biliary tree during laparoscopic cholecystectomy. Br J Surg, 2010, 97(9): 1369-1377.
14.	Landsman ML, Kwant G, Mook GA, et al. Light-absorbing properties, stability, and spectral stabilization of indocyanine green. J Appl Physiol, 1976, 40(4): 575-583.
15.	Branch RA. Drugs as indicators of hepatic function. Hepatology, 1982, 2(1): 97-105.
16.	Gotoh K, Yamada T, Ishikawa O, et al. A novel image-guided surgery of hepatocellular carcinoma by indocyanine green fluorescence imaging navigation. J Surg Oncol, 2009, 100(1): 75-79.
17.	方驰华, 方程, 田捷. 吲哚氰绿介导的近红外光检测技术在肝癌手术中的应用. 中华外科杂志, 2015, 53(2): 155-157.
18.	Ishizawa T, Mise Y, Aoki T, et al. Surgical technique: new advances for expanding indications and increasing safety in liver resection for HCC: the Eastern perspective. J Hepatobiliary Pancreat Sci, 2010, 17(4): 389-393.
19.	Lim C, Vibert E, Azoulay D, et al. Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications. J Visc Surg, 2014, 151(2): 117-124.
20.	Ishizawa T, Masuda K, Urano Y, et al. Mechanistic background and clinical applications of indocyanine green fluorescence imaging of hepatocellular carcinoma. Ann Surg Oncol, 2014, 21(2): 440-448.
21.	Yokoyama N, Otani T, Hashidate H, et al. Real-time detection of hepatic micrometastases from pancreatic cancer by intraoperative fluorescence imaging: preliminary results of a prospective study. Cancer, 2012, 118(11): 2813-2819.
22.	Harada N, Ishizawa T, Muraoka A, et al. Fluorescence navigation hepatectomy by visualization of localized cholestasis from bile duct tumor infiltration. J Am Coll Surg, 2010, 210(6): e2-e6.
23.	Kawaguchi Y, Ishizawa T, Masuda K, et al. Hepatobiliary surgery guided by a novel fluorescent imaging technique for visualizing hepatic arteries, bile ducts, and liver cancers on color images. J Am Coll Surg, 2011, 212(6): e33-e39.
24.	Kawaguchi Y, Ishizawa T, Miyata Y, et al. Portal uptake function in veno-occlusive regions evaluated by real-time fluorescent imaging using indocyanine green. J Hepatol, 2013, 58(2): 247-253.
25.	Kawaguchi Y, Ishizawa T, Kokudo N. Estimation of portal uptake function in the venous congestive area after hemi-hepatectomy: postoperative contrast-enhanced magnetic resonance imaging and intraoperative indocyanine green-fluorescence imaging. J Hepatobiliary Pancreat Sci, 2014, 21(1): e1.
26.	Yokoo H, Nakanishi K, Kakisaka T, et al. Usefulness of intraoperative fluorescent imaging using indocyanine green for repeated resection of hepatocellular carcinoma. Gan To Kagaku Ryoho, 2011, 38(12): 2481-2483.
27.	方驰华, 梁洪玻, 迟崇巍, 等. 吲哚氰绿介导的近红外光技术在微小肝脏肿瘤识别、切缘界定和精准手术导航的应用. 中华外科杂志, 2016, 54(6): 444-450.
28.	董家鸿, 刘兵, 迟崇巍, 等. 吲哚菁绿近红外荧光显像技术在肝细胞癌肝切除术中的应用价值. 中华消化外科杂志, 2016, 15(5): 490-495.
29.	Zhang YM, Shi R, Hou JC, et al. Liver tumor boundaries identified intraoperatively using real-time indocyanine green fluorescence imaging. J Cancer Res Clin Oncol, 2017, 143(1): 51-58.
30.	Kudo H, Ishizawa T, Tani K, et al. Visualization of subcapsular hepatic malignancy by indocyanine-green fluorescence imaging during laparoscopic hepatectomy. Surg Endosc, 2014, 28(8): 2504-2508.
31.	王宏光, 许寅喆, 陈明易, 等. 吲哚菁绿荧光融合影像引导在腹腔镜解剖性肝切除术中的应用价值. 中华消化外科杂志, 2017, 16(4): 405-409.
32.	陈琳, 罗鸿萍, 朱鹏, 等. 吲哚菁绿荧光实时成像技术在机器人肝切除术中的初步应用(附二例报告). 腹部外科, 2017, 30(4): 254-257.
33.	Satou S, Ishizawa T, Masuda K, et al. Indocyanine green fluorescent imaging for detecting extrahepatic metastasis of hepatocellular carcinoma. J Gastroenterol, 2013, 48(10): 1136-1143.
34.	Morita Y, Sakaguchi T, Unno N, et al. Detection of hepatocellular carcinomas with near-infrared fluorescence imaging using indocyanine green: its usefulness and limitation. Int J Clin Oncol, 2013, 18(2): 232-241.
35.	Kitai T, Miwa M, Liu H, et al. Application of near-infrared time-resolved spectroscopy to rat liver--a preliminary report for surgical application. Phys Med Biol, 1999, 44(8): 2049-2061.

1. Llovet JM, Bruix J. Novel advancements in the management of hepatocellular carcinoma in 2008. J Hepatol, 2008, 48 Suppl 1: S20-S37.
2. Ishizawa T, Fukushima N, Shibahara J, et al. Real-time identification of liver cancers by using indocyanine green fluorescent imaging. Cancer, 2009, 115(11): 2491-2504.
3. Herschman HR. Molecular imaging: looking at problems, seeing solutions. Science, 2003, 302(5645): 605-608.
4. Jaffer FA, Weissleder R. Molecular imaging in the clinical arena. JAMA, 2005, 293(7): 855-862.
5. Benson RC, Kues HA. Fluorescence properties of indocyanine green as related to angiography. Phys Med Biol, 1978, 23(1): 159-163.
6. Morton CA, Brown SB, Collins S, et al. Guidelines for topical photodynamic therapy: report of a workshop of the British Photodermatology Group. Br J Dermatol, 2002, 146(4): 552-567.
7. Stummer W, Stocker S, Wagner S, et al. Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery, 1998, 42(3): 518-525.
8. Unno N, Inuzuka K, Suzuki M, et al. Preliminary experience with a novel fluorescence lymphography using indocyanine green in patients with secondary lymphedema. J Vasc Surg, 2007, 45(5): 1016-1021.
9. Unno N, Suzuki M, Yamamoto N, et al. Indocyanine green fluorescence angiography for intraoperative assessment of blood flow: a feasibility study. Eur J Vasc Endovasc Surg, 2008, 35(2): 205-207.
10. Lam B, Wong MP, Fung SL, et al. The clinical value of autofluorescence bronchoscopy for the diagnosis of lung cancer. Eur Respir J, 2006, 28(5): 915-919.
11. Kusano M, Tajima Y, Yamazaki K, et al. Sentinel node mapping guided by indocyanine green fluorescence imaging: a new method for sentinel node navigation surgery in gastrointestinal cancer. Dig Surg, 2008, 25(2): 103-108.
12. Ishizawa T, Tamura S, Masuda K, et al. Intraoperative fluorescent cholangiography using indocyanine green: a biliary road map for safe surgery. J Am Coll Surg, 2009, 208(1): e1-e4.
13. Ishizawa T, Bandai Y, Ijichi M, et al. Fluorescent cholangiography illuminating the biliary tree during laparoscopic cholecystectomy. Br J Surg, 2010, 97(9): 1369-1377.
14. Landsman ML, Kwant G, Mook GA, et al. Light-absorbing properties, stability, and spectral stabilization of indocyanine green. J Appl Physiol, 1976, 40(4): 575-583.
15. Branch RA. Drugs as indicators of hepatic function. Hepatology, 1982, 2(1): 97-105.
16. Gotoh K, Yamada T, Ishikawa O, et al. A novel image-guided surgery of hepatocellular carcinoma by indocyanine green fluorescence imaging navigation. J Surg Oncol, 2009, 100(1): 75-79.
17. 方驰华, 方程, 田捷. 吲哚氰绿介导的近红外光检测技术在肝癌手术中的应用. 中华外科杂志, 2015, 53(2): 155-157.
18. Ishizawa T, Mise Y, Aoki T, et al. Surgical technique: new advances for expanding indications and increasing safety in liver resection for HCC: the Eastern perspective. J Hepatobiliary Pancreat Sci, 2010, 17(4): 389-393.
19. Lim C, Vibert E, Azoulay D, et al. Indocyanine green fluorescence imaging in the surgical management of liver cancers: current facts and future implications. J Visc Surg, 2014, 151(2): 117-124.
20. Ishizawa T, Masuda K, Urano Y, et al. Mechanistic background and clinical applications of indocyanine green fluorescence imaging of hepatocellular carcinoma. Ann Surg Oncol, 2014, 21(2): 440-448.
21. Yokoyama N, Otani T, Hashidate H, et al. Real-time detection of hepatic micrometastases from pancreatic cancer by intraoperative fluorescence imaging: preliminary results of a prospective study. Cancer, 2012, 118(11): 2813-2819.
22. Harada N, Ishizawa T, Muraoka A, et al. Fluorescence navigation hepatectomy by visualization of localized cholestasis from bile duct tumor infiltration. J Am Coll Surg, 2010, 210(6): e2-e6.
23. Kawaguchi Y, Ishizawa T, Masuda K, et al. Hepatobiliary surgery guided by a novel fluorescent imaging technique for visualizing hepatic arteries, bile ducts, and liver cancers on color images. J Am Coll Surg, 2011, 212(6): e33-e39.
24. Kawaguchi Y, Ishizawa T, Miyata Y, et al. Portal uptake function in veno-occlusive regions evaluated by real-time fluorescent imaging using indocyanine green. J Hepatol, 2013, 58(2): 247-253.
25. Kawaguchi Y, Ishizawa T, Kokudo N. Estimation of portal uptake function in the venous congestive area after hemi-hepatectomy: postoperative contrast-enhanced magnetic resonance imaging and intraoperative indocyanine green-fluorescence imaging. J Hepatobiliary Pancreat Sci, 2014, 21(1): e1.
26. Yokoo H, Nakanishi K, Kakisaka T, et al. Usefulness of intraoperative fluorescent imaging using indocyanine green for repeated resection of hepatocellular carcinoma. Gan To Kagaku Ryoho, 2011, 38(12): 2481-2483.
27. 方驰华, 梁洪玻, 迟崇巍, 等. 吲哚氰绿介导的近红外光技术在微小肝脏肿瘤识别、切缘界定和精准手术导航的应用. 中华外科杂志, 2016, 54(6): 444-450.
28. 董家鸿, 刘兵, 迟崇巍, 等. 吲哚菁绿近红外荧光显像技术在肝细胞癌肝切除术中的应用价值. 中华消化外科杂志, 2016, 15(5): 490-495.
29. Zhang YM, Shi R, Hou JC, et al. Liver tumor boundaries identified intraoperatively using real-time indocyanine green fluorescence imaging. J Cancer Res Clin Oncol, 2017, 143(1): 51-58.
30. Kudo H, Ishizawa T, Tani K, et al. Visualization of subcapsular hepatic malignancy by indocyanine-green fluorescence imaging during laparoscopic hepatectomy. Surg Endosc, 2014, 28(8): 2504-2508.
31. 王宏光, 许寅喆, 陈明易, 等. 吲哚菁绿荧光融合影像引导在腹腔镜解剖性肝切除术中的应用价值. 中华消化外科杂志, 2017, 16(4): 405-409.
32. 陈琳, 罗鸿萍, 朱鹏, 等. 吲哚菁绿荧光实时成像技术在机器人肝切除术中的初步应用(附二例报告). 腹部外科, 2017, 30(4): 254-257.
33. Satou S, Ishizawa T, Masuda K, et al. Indocyanine green fluorescent imaging for detecting extrahepatic metastasis of hepatocellular carcinoma. J Gastroenterol, 2013, 48(10): 1136-1143.
34. Morita Y, Sakaguchi T, Unno N, et al. Detection of hepatocellular carcinomas with near-infrared fluorescence imaging using indocyanine green: its usefulness and limitation. Int J Clin Oncol, 2013, 18(2): 232-241.
35. Kitai T, Miwa M, Liu H, et al. Application of near-infrared time-resolved spectroscopy to rat liver--a preliminary report for surgical application. Phys Med Biol, 1999, 44(8): 2049-2061.

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The clinical application and progress of indocyanine green-fluorescence imaging in liver tumor surgery

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