Advertisement

Surgery Today

, Volume 45, Issue 12, pp 1467–1474 | Cite as

Recent advances in near-infrared fluorescence-guided imaging surgery using indocyanine green

  • Tsutomu NamikawaEmail author
  • Takayuki Sato
  • Kazuhiro Hanazaki
Review Article

Abstract

Near-infrared (NIR) fluorescence imaging has better tissue penetration, allowing for the effective rejection of excitation light and detection deep inside organs. Indocyanine green (ICG) generates NIR fluorescence after illumination by an NIR ray, enabling real-time intraoperative visualization of superficial lymphatic channels and vessels transcutaneously. The HyperEye Medical System (HEMS) can simultaneously detect NIR rays under room light to provide color imaging, which enables visualization under bright light. Thus, NIR fluorescence imaging using ICG can provide for excellent diagnostic accuracy in detecting sentinel lymph nodes in cancer and microvascular circulation in various ischemic diseases, to assist us with intraoperative decision making. Including HEMS in this system could further improve the sentinel lymph node mapping and intraoperative identification of blood supply in reconstructive organs and ischemic diseases, making it more attractive than conventional imaging. Moreover, the development of new laparoscopic imaging systems equipped with NIR will allow fluorescence-guided surgery in a minimally invasive setting. Future directions, including the conjugation of NIR fluorophores to target specific cancer markers might be realistic technology with diagnostic and therapeutic benefits.

Keywords

HyperEye Medical System Indocyanine green Fluorescence imaging Navigation surgery Near-infrared fluorescence 

Notes

Conflict of interest

None.

References

  1. 1.
    Schaafsma BE, Mieog JS, Hutteman M, van der Vorst JR, Kuppen PJ, Löwik CW, et al. The clinical use of indocyanine green as a near-infrared fluorescent contrast agent for image-guided oncologic surgery. J Surg Oncol. 2011;104:323–32.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Gioux S, Choi HS, Frangioni JV. Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation. Mol Imaging. 2010;9:237–55.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Ogawa M, Kosaka N, Choyke PL, Kobayashi H. In vivo molecular imaging of cancer with a quenching near-infrared fluorescent probe using conjugates of monoclonal antibodies and indocyanine green. Cancer Res. 2009;69:1268–72.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Ogata F, Azuma R, Kikuchi M, Koshima I, Morimoto Y. Novel lymphography using indocyanine green dye for near-infrared fluorescence labeling. Ann Plast Surg. 2007;58:652–5.CrossRefPubMedGoogle Scholar
  5. 5.
    Murawa D, Polom K, Murawa P. One-year postoperative morbidity associated with near-infrared-guided indocyanine green (ICG) or ICG in conjugation with human serum albumin (ICG:HSA) sentinel lymph node biopsy. Surg Innov. 2013;21:240–3.CrossRefPubMedGoogle Scholar
  6. 6.
    Yamamoto M, Orihashi K, Nishimori H, Handa T, Kondo N, Fukutomi T, et al. Efficacy of intraoperative HyperEye Medical System angiography for coronary artery bypass grafting. Surg Today. 2014 (Epub ahead of print)Google Scholar
  7. 7.
    Handa T, Katare RG, Nishimori H, Wariishi S, Fukutomi T, Yamamoto M, et al. New device for intraoperative graft assessment: HyperEye charge-coupled device camera system. Gen Thorac Cardiovasc Surg. 2010;58:68–77.CrossRefPubMedGoogle Scholar
  8. 8.
    Handa T, Katare RG, Sasaguri S, Sato T. Preliminary experience for the evaluation of the intraoperative graft patency with real color charge-coupled device camera system: an advanced device for simultaneous capturing of color and near-infrared images during coronary artery bypass graft. Interact CardioVasc Thorac Surg. 2009;9:150–4.CrossRefPubMedGoogle Scholar
  9. 9.
    Yamamoto M, Sasaguri S, Sato T. Assessing intraoperative blood flow in cardiovascular surgery. Surg Today. 2011;41:1467–74.CrossRefPubMedGoogle Scholar
  10. 10.
    Yamamoto M, Orihashi K, Nishimori H, Wariishi S, Fukutomi T, Kondo N, et al. Indocyanine green angiography for intra-operative assessment in vascular surgery. Eur J Vasc Endovasc Surg. 2012;43:426–32.CrossRefPubMedGoogle Scholar
  11. 11.
    Giuliano AE, Hunt KK, Ballman KV, Beitsch PD, Whitworth PW, Blumencranz PW, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA. 2011;305:569–75.CrossRefPubMedGoogle Scholar
  12. 12.
    Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Costantino JP, et al. Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol. 2010;11:927–33.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Ashikaga T, et al. Technical outcomes of sentinel-lymph-node resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial. Lancet Oncol. 2007;8:881–8.CrossRefPubMedGoogle Scholar
  14. 14.
    Cox CE, Pendas S, Cox JM, Joseph E, Shons AR, Yeatman T, et al. Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg. 1998;227:645–53.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Zavagno G, De Salvo GL, Scalco G, Bozza F, Barutta L, Del Bianco P, et al. A Randomized clinical trial on sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer: results of the Sentinella/GIVOM trial. Ann Surg. 2008;247:207–13.CrossRefPubMedGoogle Scholar
  16. 16.
    Tafra L, Lannin DR, Swanson MS, Van Eyk JJ, Verbanac KM, Chua AN, et al. Multicenter trial of sentinel node biopsy for breast cancer using both technetium sulfur colloid and isosulfan blue dye. Ann Surg. 2001;233:51–9.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Nimura H, Narimiya N, Mitsumori N, Yamazaki Y, Yanaga K, Urashima M. Infrared ray electronic endoscopy combined with indocyanine green injection for detection of sentinel nodes of patients with gastric cancer. Br J Surg. 2004;91:575–9.CrossRefPubMedGoogle Scholar
  18. 18.
    Kitai T, Inomoto T, Miwa M, Shikayama T. Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer. 2005;12:211–5.CrossRefPubMedGoogle Scholar
  19. 19.
    Tagaya N, Yamazaki R, Nakagawa A, Abe A, Hamada K, Kubota K, et al. Intraoperative identification of sentinel lymph nodes by near-infrared fluorescence imaging in patients with breast cancer. Am J Surg. 2008;195:850–3.CrossRefPubMedGoogle Scholar
  20. 20.
    Murawa D, Hirche C, Dresel S, Hünerbein M. Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence. Br J Surg. 2009;96:1289–94.CrossRefPubMedGoogle Scholar
  21. 21.
    Troyan SL, Kianzad V, Gibbs-Strauss SL, Gioux S, Matsui A, Oketokoun R, et al. The FLARE intraoperative near-infrared fluorescence imaging system: a first-in-human clinical trial in breast cancer sentinel lymph node mapping. Ann Surg Oncol. 2009;16:2943–52.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Hirche C, Murawa D, Mohr Z, Kneif S, Hünerbein M. ICG fluorescence-guided sentinel node biopsy for axillary nodal staging in breast cancer. Breast Cancer Res Treat. 2010;121:373–8.CrossRefPubMedGoogle Scholar
  23. 23.
    Hojo T, Nagao T, Kikuyama M, Akashi S, Kinoshita T. Evaluation of sentinel node biopsy by combined fluorescent and dye method and lymph flow for breast cancer. Breast. 2010;19:210–3.CrossRefPubMedGoogle Scholar
  24. 24.
    Mieog JS, Troyan SL, Hutteman M, Donohoe KJ, van der Vorst JR, Stockdale A, et al. Toward optimization of imaging system and lymphatic tracer for near-infrared fluorescent sentinel lymph node mapping in breast cancer. Ann Surg Oncol. 2011;18:2483–91.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Tagaya N, Aoyagi H, Nakagawa A, Abe A, Iwasaki Y, Tachibana M, et al. A novel approach for sentinel lymph node identification using fluorescence imaging and image overlay navigation surgery in patients with breast cancer. World J Surg. 2011;35:154–8.CrossRefPubMedGoogle Scholar
  26. 26.
    van der Vorst JR, Schaafsma BE, Verbeek FP, Hutteman M, Mieog JS, Lowik CW, et al. Randomized comparison of near-infrared fluorescence imaging using indocyanine green and 99 (m) technetium with or without patent blue for the sentinel lymph node procedure in breast cancer patients. Ann Surg Oncol. 2012;19:4104–11.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Schaafsma BE, Verbeek FP, Rietbergen DD, van der Hiel B, van der Vorst JR, Liefers GJ, et al. Clinical trial of combined radio- and fluorescence-guided sentinel lymph node biopsy in breast cancer. Br J Surg. 2013;100:1037–44.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Guo W, Zhang L, Ji J, Gao W, Liu J, Tong M. Evaluation of the benefit of using blue dye in addition to indocyanine green fluorescence for sentinel lymph node biopsy in patients with breast cancer. World J Surg Oncol. 2014;12:290.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Tong M, Guo W, Gao W. Use of fluorescence imaging in combination with patent blue dye versus patent blue dye alone in sentinel lymph node biopsy in breast cancer. J Breast Cancer. 2014;17:250–5.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Ogasawara Y, Ikeda H, Takahashi M, Kawasaki K, Doihara H. Evaluation of breast lymphatic pathways with indocyanine green fluorescence imaging in patients with breast cancer. World J Surg. 2008;32:1924–9.CrossRefPubMedGoogle Scholar
  31. 31.
    Fujisawa Y, Nakamura Y, Kawachi Y, Otsuka F. Indocyanine green fluorescence-navigated sentinel node biopsy showed higher sensitivity than the radioisotope or blue dye method, which may help to reduce false-negative cases in skin cancer. J Surg Oncol. 2012;106:41–5.CrossRefPubMedGoogle Scholar
  32. 32.
    Cloyd JM, Wapnir IL, Read BM, Swetter S, Greco RS. Indocyanine green and fluorescence lymphangiography for sentinel lymph node identification in cutaneous melanoma. J Surg Oncol. 2014;110:888–92 (Epub ahead of print).CrossRefPubMedGoogle Scholar
  33. 33.
    Tajima Y, Yamazaki K, Masuda Y, Kato M, Yasuda D, Aoki T, et al. Sentinel node mapping guided by indocyanine green fluorescence imaging in gastric cancer. Ann Surg. 2009;249:58–62.CrossRefPubMedGoogle Scholar
  34. 34.
    Schaafsma BE, Verbeek FP, Elzevier HW, Tummers QR, van der Vorst JR, Frangioni JV, et al. Optimization of sentinel lymph node mapping in bladder cancer using near-infrared fluorescence imaging. J Surg Oncol. 2014;110:845–50.CrossRefPubMedGoogle Scholar
  35. 35.
    Yamauchi K, Nagafuji H, Nakamura T, Sato T, Kohno N. Feasibility of ICG fluorescence-guided sentinel node biopsy in animal models using the HyperEye Medical System. Ann Surg Oncol. 2011;18:2042–7.CrossRefPubMedGoogle Scholar
  36. 36.
    Frangioni JV. In vivo near-infrared fluorescence imaging. Curr Opin Chem Biol. 2003;7:626–34.CrossRefPubMedGoogle Scholar
  37. 37.
    Unno N, Suzuki M, Yamamoto N, Inuzuka K, Sagara D, Nishiyama M, et al. Indocyanine green fluorescence angiography for intraoperative assessment of blood flow: a feasibility study. Eur J Vasc Endovasc Surg. 2008;35:205–7.CrossRefPubMedGoogle Scholar
  38. 38.
    Champagne BJ, Lee EC, Valerian B, Mulhotra N, Mehta M. Incidence of colonic ischemia after repair of ruptured abdominal aortic aneurysm with endograft. J Am Coll Surg. 2007;204:597–602.CrossRefPubMedGoogle Scholar
  39. 39.
    Champagne BJ, Darling RC, Daneshmand M, Kreienberg PB, Lee EC, Mehta M, Roddy SP, Chang BB, Paty PS, Ozsvath KJ, Shah DM. Outcome of aggressive surveillance colonoscopy in ruptured abdominal aortic aneurysm. J Vasc Surg. 2004;39:792–6.CrossRefPubMedGoogle Scholar
  40. 40.
    Rino Y, Yukawa N, Sato T, Yamamoto N, Tamagawa H, Hasegawa S, et al. Visualization of blood supply route to the reconstructed stomach by indocyanine green fluorescence imaging during esophagectomy. BMC Med Imaging. 2014;14:18.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Kubota K, Yoshida M, Kuroda J, Okada A, Ohta K, Kitajima M. Application of the HyperEye Medical System for esophageal cancer surgery: a preliminary report. Surg Today. 2013;43:215–20.CrossRefPubMedGoogle Scholar
  42. 42.
    Tajima Y, Murakami M, Yamazaki K, Masuda Y, Kato M, Sato A, et al. Sentinel node mapping guided by indocyanine green fluorescence imaging during laparoscopic surgery in gastric cancer. Ann Surg Oncol. 2010;17:1787–93.CrossRefPubMedGoogle Scholar
  43. 43.
    Morita K, Ishizawa T, Tani K, Harada N, Shimizu A, Yamamoto S, et al. Application of indocyanine green-fluorescence imaging to full-thickness cholecystectomy. Asian J Endosc Surg. 2014;7:193–5.CrossRefPubMedGoogle Scholar
  44. 44.
    Mazzei MA, Mazzei FG, Marrelli D, Imbriaco G, Guerrini S, Vindigni C, et al. Computed tomographic evaluation of mesentery: diagnostic value in acute mesenteric ischemia. J Comput Assist Tomogr. 2012;36:1–7.CrossRefPubMedGoogle Scholar
  45. 45.
    Boni L, David G, Mangano A, Dionigi G, Rausei S, Spampatti S, et al. Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc. 2014 (Epub ahead of print)Google Scholar
  46. 46.
    Verbeek FP, Schaafsma BE, Tummers QR, van der Vorst JR, van der Made WJ, Baeten CI, et al. Optimization of near-infrared fluorescence cholangiography for open and laparoscopic surgery. Surg Endosc. 2014;28(4):1076–82.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Yasuhara H. Acute mesenteric ischemia: the challenge of gastroenterology. Surg Today. 2005;35:185–95.CrossRefPubMedGoogle Scholar
  48. 48.
    Yukaya T, Saeki H, Taketani K, Ando K, Ida S, Kimura Y, et al. Clinical outcomes and prognostic factors after surgery for non-occlusive mesenteric ischemia: a multicenter study. J Gastrointest Surg. 2014;18:1642–7.CrossRefPubMedGoogle Scholar
  49. 49.
    John AS, Tuerff SD, Kerstein MD. Nonocclusive mesenteric infarction in hemodialysis patients. J Am Coll Surg. 2000;190:84–8.CrossRefPubMedGoogle Scholar
  50. 50.
    Firetto MC, Lemos AA, Marini A, Avesani EC, Biondetti PR. Acute bowel ischemia: analysis of diagnostic error by overlooked findings at MDCT angiography. Emerg Radiol. 2013;20:139–47.CrossRefPubMedGoogle Scholar
  51. 51.
    Nitori N, Deguchi T, Kubota K, Yoshida M, Kato A, Kojima M, et al. Successful treatment of non-occlusive mesenteric ischemia (NOMI) using the HyperEye Medical System™ for intraoperative visualization of the mesenteric and bowel circulation: report of a case. Surg Today. 2014;44:359–62.CrossRefPubMedGoogle Scholar
  52. 52.
    Namikawa T, Uemura S, Kondo N, Yamamoto M, Maeda H, Nishimori H, et al. Successful preservation of the mesenteric and bowel circulation with treatment for a ruptured superior mesenteric artery aneurysm using the HyperEye Medical System. Am Surg. 2014;80:359–61.Google Scholar
  53. 53.
    Gotoh K, Yamada T, Ishikawa O, Takahashi H, Eguchi H, Yano M, et al. A novel image-guided surgery of hepatocellular carcinoma by indocyanine green fluorescence imaging navigation. J Surg Oncol. 2009;100:75–9.CrossRefPubMedGoogle Scholar
  54. 54.
    Ishizawa T, Fukushima N, Shibahara J, Masuda K, Tamura S, Aoki T, et al. Real-time identification of liver cancers by using indocyanine green fluorescent imaging. Cancer. 2009;115:2491–504.CrossRefPubMedGoogle Scholar
  55. 55.
    van der Vorst JR, Schaafsma BE, Hutteman M, Verbeek FP, Liefers GJ, Hartgrink HH, et al. Near-infrared fluorescence-guided resection of colorectal liver metastases. Cancer. 2013;119:3411–8.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Verbeek FP, van der Vorst JR, Schaafsma BE, Hutteman M, Bonsing BA, van Leeuwen FW, et al. Image-guided hepatopancreatobiliary surgery using near-infrared fluorescent light. J Hepatobiliary Pancreat Sci. 2012;19:626–37.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Morita Y, Sakaguchi T, Unno N, Shibasaki Y, Suzuki A, Fukumoto K, et al. Detection of hepatocellular carcinomas with near-infrared fluorescence imaging using indocyanine green: its usefulness and limitation. Int J Clin Oncol. 2013;18:232–41.CrossRefPubMedGoogle Scholar
  58. 58.
    Ashitate Y, Stockdale A, Choi HS, Laurence RG, Frangioni JV. Real-time simultaneous near-infrared fluorescence imaging of bile duct and arterial anatomy. J Surg Res. 2012;176:7–13.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Matsui A, Tanaka E, Choi HS, Winer JH, Kianzad V, Gioux S, et al. Real-time intra-operative near-infrared fluorescence identification of the extrahepatic bile ducts using clinically available contrast agents. Surgery. 2010;148:87–95.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Sevick-Muraca EM, Sharma R, Rasmussen JC, Marshall MV, Wendt JA, Pham HQ, et al. Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study. Radiology. 2008;246:734–41.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Namikawa T, Inoue K, Uemura S, Shiga M, Maeda H, Kitagawa H, et al. Photodynamic diagnosis using 5-aminolevulinic acid during gastrectomy for gastric cancer. J Surg Oncol. 2014;109:213–7.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Japan 2015

Authors and Affiliations

  • Tsutomu Namikawa
    • 1
    Email author
  • Takayuki Sato
    • 2
  • Kazuhiro Hanazaki
    • 1
  1. 1.Department of SurgeryKochi Medical SchoolNankokuJapan
  2. 2.Department of Cardiovascular ControlKochi Medical SchoolNankokuJapan

Personalised recommendations