Skip to main content
SpringerLink
Log in

Optimization of near-infrared fluorescence cholangiography for open and laparoscopic surgery

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

During laparoscopic cholecystectomy, common bile duct (CBD) injury is a rare but severe complication. To reduce the risk of injury, near-infrared (NIR) fluorescent cholangiography using indocyanine green (ICG) has recently been introduced as a novel method of visualizing the biliary system during surgery. To date, several studies have shown feasibility of this technique; however, liver background fluorescence remains a major problem during fluorescent cholangiography. The aim of the current study was to optimize ICG dose and timing for NIR cholangiography using a quantitative intraoperative camera system during open hepatopancreatobiliary (HPB) surgery. Subsequently, these results were validated during laparoscopic cholecystectomy using a laparoscopic fluorescence imaging system.

Methods

Twenty-seven patients who underwent NIR imaging using the Mini-FLARE image-guided surgery system during open HPB surgery were analyzed to assess optimal dosage and timing of ICG administration. ICG was intravenously injected preoperatively at doses of 5, 10, and 20 mg, and imaged at either 30 min (early) or 24 h (delayed) post-injection. Next, the optimal doses found for early and delayed imaging were applied to two groups of seven patients (n = 14) undergoing laparoscopic NIR fluorescent cholangiography during laparoscopic cholecystectomy.

Results

Median liver-to-background contrast was 23.5 (range 22.1–35.0), 16.8 (range 11.3–25.1), 1.3 (range 0.7–7.8), and 2.5 (range 1.3–3.6) for 5 mg/30 min, 10 mg/30 min, 10 mg/24 h, and 20 mg/24 h, respectively. Fluorescence intensity of the liver was significantly lower in the 10 mg delayed-imaging dose group compared with the early imaging 5 and 10 mg dose groups (p = 0.001), which resulted in a significant increase in CBD-to-liver contrast ratio compared with the early administration groups (p < 0.002). These findings were qualitatively confirmed during laparoscopic cholecystectomy.

Conclusion

This study shows that a prolonged interval between ICG administration and surgery permits optimal NIR cholangiography with minimal liver background fluorescence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. NIH Consensus conference. Gallstones and laparoscopic cholecystectomy. JAMA 269:1018–1024(1993)

    Google Scholar 

  2. Perissat J (1993) Laparoscopic cholecystectomy: the European experience. Am J Surg 165:444–449

    Article  CAS  PubMed  Google Scholar 

  3. Deziel DJ, Millikan KW, Economou SG, Doolas A, Ko ST, Airan MC (1993) Complications of laparoscopic cholecystectomy: a national survey of 4,292 hospitals and an analysis of 77,604 cases. Am J Surg 165:9–14

    Article  CAS  PubMed  Google Scholar 

  4. Flum DR, Koepsell T, Heagerty P, Sinanan M, Dellinger EP (2001) Common bile duct injury during laparoscopic cholecystectomy and the use of intraoperative cholangiography: adverse outcome or preventable error? Arch Surg 136:1287–1292

    Article  CAS  PubMed  Google Scholar 

  5. Giger U, Ouaissi M, Schmitz SF, Krahenbuhl S, Krahenbuhl L (2011) Bile duct injury and use of cholangiography during laparoscopic cholecystectomy. Br J Surg 98:391–396

    Article  CAS  PubMed  Google Scholar 

  6. Flum DR, Dellinger EP, Cheadle A, Chan L, Koepsell T (2003) Intraoperative cholangiography and risk of common bile duct injury during cholecystectomy. JAMA 289:1639–1644

    Article  PubMed  Google Scholar 

  7. Ford JA, Soop M, Du J, Loveday BP, Rodgers M (2012) Systematic review of intraoperative cholangiography in cholecystectomy. Br J Surg 99:160–167

    Article  CAS  PubMed  Google Scholar 

  8. Ausania F, Holmes LR, Ausania F, Iype S, Ricci P, White SA (2012) Intraoperative cholangiography in the laparoscopic cholecystectomy era: why are we still debating? Surg Endosc 26:1193–1200

    Article  CAS  PubMed  Google Scholar 

  9. Ishizawa T, Bandai Y, Ijichi M, Kaneko J, Hasegawa K, Kokudo N (2010) Fluorescent cholangiography illuminating the biliary tree during laparoscopic cholecystectomy. Br J Surg 97:1369–1377

    Article  CAS  PubMed  Google Scholar 

  10. Aoki T, Murakami M, Yasuda D, Shimizu Y, Kusano T, Matsuda K, Niiya T, Kato H, Murai N, Otsuka K, Kusano M, Kato T (2009) Intraoperative fluorescent imaging using indocyanine green for liver mapping and cholangiography. J Hepatobiliary Pancreat Surg 17:590–594

    Article  Google Scholar 

  11. Schols RM, Bouvy ND, Masclee AA, van Dam RM, Dejong CH, Stassen LP (2013) Fluorescence cholangiography during laparoscopic cholecystectomy: a feasibility study on early biliary tract delineation. Surg Endosc 27:1530–1536

    Article  PubMed  Google Scholar 

  12. Cherrick GR, Stein SW, Leevy CM, Davidson CS (1960) Indocyanine green: observations on its physical properties, plasma decay, and hepatic extraction. J Clin Invest 39:592–600

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Schols RM, Bouvy ND, van Dam RM, Stassen LP (2013) Advanced intraoperative imaging methods for laparoscopic anatomy navigation: an overview. Surg Endosc 27:1851–1859

    Article  PubMed  Google Scholar 

  14. Gioux S, Choi HS, Frangioni JV (2010) Image-guided surgery using invisible near-infrared light: fundamentals of clinical translation. Mol Imaging 9:237–255

    CAS  PubMed Central  PubMed  Google Scholar 

  15. Verbeek FP, van der Vorst JR, Schaafsma BE, Hutteman M, Bonsing BA, van Leeuwen FW, Frangioni JV, van de Velde CJ, Swijnenburg RJ, Vahrmeijer AL (2012) Image-guided hepatopancreatobiliary surgery using near-infrared fluorescent light. J Hepatobiliary Pancreat Sci 19:626–637

    Article  PubMed Central  PubMed  Google Scholar 

  16. Mieog JS, Troyan SL, Hutteman M, Donohue KJ, van der Vorst JR, Stockdale A, Liefers GJ, Choi HS, Gibbs-Strauss SL, Putter H, Gioux S, Kuppen PJ, Ashitate Y, Löwik CW, Smit VT, Oketokoun R, Ngo LH, van de Velde CJ, Frangioni JV, Vahrmeijer AL (2011) Towards optimization of imaging system and lymphatic tracer for near-infrared fluorescent sentinel lymph node mapping in breast cancer. Ann Surg Oncol 18:2483–2491

    Article  PubMed Central  PubMed  Google Scholar 

  17. Tanaka E, Choi HS, Humblet V, Ohnishi S, Laurence RG, Frangioni JV (2008) Real-time intraoperative assessment of the extrahepatic bile ducts in rats and pigs using invisible near-infrared fluorescent light. Surgery 144:39–48

    Article  PubMed Central  PubMed  Google Scholar 

  18. Hutteman M, van der Vorst JR, Mieog JS, Bonsing BA, Hartgrink HH, Kuppen PJ, Lowik CW, Frangioni JV, van de Velde CJ, Vahrmeijer AL (2011) Near-infrared fluorescence imaging in patients undergoing pancreaticoduodenectomy. Eur Surg Res 47:90–97

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. 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 15:508–514

    Article  PubMed  Google Scholar 

  20. Mizuno S, Isaji S (2010) Indocyanine green (ICG) fluorescence imaging-guided cholangiography for donor hepatectomy in living donor liver transplantation. Am J Transplant 10:2725–2726

    Article  CAS  PubMed  Google Scholar 

  21. Ishizawa T, Tamura S, Masuda K, Aoki T, Hasegawa K, Imamura H, Beck Y, Kokudo N (2009) Intraoperative fluorescent cholangiography using indocyanine green: a biliary road map for safe surgery. J Am Coll Surg 208:e1–e4

    Article  PubMed  Google Scholar 

  22. Ishizawa T, Bandai Y, Kokudo N (2009) Fluorescent cholangiography using indocyanine green for laparoscopic cholecystectomy: an initial experience. Arch Surg 144:381–382

    Article  PubMed  Google Scholar 

  23. Kawaguchi Y, Ishizawa T, Masuda K, Sato S, Kaneko J, Aoki T, Beck Y, Sugawara Y, Hasegawa K, Kokudo N (2011) 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 212:e33–e39

    Article  PubMed  Google Scholar 

  24. Tagaya N, Shimoda M, Kato M, Nakagawa A, Abe A, Iwasaki Y, Oishi H, Shirotani N, Kubota K (2009) Intraoperative exploration of biliary anatomy using fluorescence imaging of indocyanine green in experimental and clinical cholecystectomies. J Hepatobiliary Pancreat Surg 17:595–600

    Article  Google Scholar 

  25. Ishizawa T, Kaneko J, Inoue Y, Takemura N, Seyama Y, Aoki T, Beck Y, Sugawara Y, Hasegawa K, Harada N, Ijichi M, Kusaka K, Shibasaki M, Bandai Y, Kokudo N (2011) Application of fluorescent cholangiography to single-incision laparoscopic cholecystectomy. Surg Endosc 25:2631–2636

    Article  PubMed  Google Scholar 

  26. Buchs NC, Pugin F, Azagury DE, Jung M, Volonte F, Hagen ME, Morel P (2013) Real-time near-infrared fluorescent cholangiography could shorten operative time during robotic single-site cholecystectomy. Surg Endosc 27:3897–3901

    Article  PubMed  Google Scholar 

  27. Ashitate Y, Stockdale A, Choi HS, Laurence RG, Frangioni JV (2011) Real-time simultaneous near-infrared fluorescence imaging of bile duct and arterial anatomy. J Surg Res 176(1):7–13

    Article  PubMed Central  PubMed  Google Scholar 

  28. Matsui A, Tanaka E, Choi HS, Winer JH, Kianzad V, Gioux S, Laurence RG, Frangioni JV (2010) Real-time intra-operative near-infrared fluorescence identification of the extrahepatic bile ducts using clinically available contrast agents. Surgery 148:87–95

    Article  PubMed Central  PubMed  Google Scholar 

  29. Sherwinter DA (2012) Identification of anomolous biliary anatomy using near-infrared cholangiography. J Gastrointest Surg 16:1814–1815

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank David Burrington Jr. for editing this manuscript. This work was supported in part by the Dutch Cancer Society Grant UL2010-4732. Research reported in this publication was also supported by the National Institutes of Health grant R01-CA-115296.

Disclosures

Dr. John V. Frangioni declares the following: FLARE™ technology is owned by Beth Israel Deaconess Medical Center, a teaching hospital of Harvard Medical School. It has been licensed to the FLARE™ Foundation, a non-profit organization focused on promoting the dissemination of medical imaging technology for research and clinical use. Dr. Frangioni is the founder and chairman of the FLARE™ Foundation. The Beth Israel Deaconess Medical Center will receive royalties for the sale of FLARE™ Technology. Dr. Frangioni has elected to surrender post-market royalties to which he would otherwise be entitled as inventor, and has elected to donate pre-market proceeds to the FLARE™ Foundation. Floris P. R. Verbeek, Boudewijn E. Schaafsma, Quirijn R.J.G. Tummers, Joost R. van der Vorst, Wendeline J. van der Made, Coen I. Baeten, Bert A. Bonsing, Cornelius J. H. van de Velde, Alexander L. Vahrmeijer and Rutger-Jan Swijnenburg have no conflicts of interest or financial ties to disclose.

Disclaimer

The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Author information

Authors and Affiliations

  1. Department of Surgery, Leiden University Medical Center, Albinusdreef 2, RC 2300, Leiden, The Netherlands

    Floris P. R. Verbeek, Boudewijn E. Schaafsma, Quirijn R. J. G. Tummers, Joost R. van der Vorst, Wendeline J. van der Made, Coen I. M. Baeten, Bert A. Bonsing, Cornelis J. H. van de Velde, Alexander L. Vahrmeijer & Rutger-Jan Swijnenburg

  2. Department of Radiology, Beth Israel Deaconess Medical Center, Boston, MA, USA

    John V. Frangioni

  3. Division of Hematology/Oncology, Department of Medicine, Beth Israel Deaconess Medical Center, Boston, MA, USA

    John V. Frangioni

Authors
  1. Floris P. R. Verbeek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Boudewijn E. Schaafsma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Quirijn R. J. G. Tummers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joost R. van der Vorst
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wendeline J. van der Made
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Coen I. M. Baeten
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bert A. Bonsing
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. John V. Frangioni
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Cornelis J. H. van de Velde
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Alexander L. Vahrmeijer
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Rutger-Jan Swijnenburg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander L. Vahrmeijer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verbeek, F.P.R., Schaafsma, B.E., Tummers, Q.R.J.G. et al. Optimization of near-infrared fluorescence cholangiography for open and laparoscopic surgery. Surg Endosc 28, 1076–1082 (2014). https://doi.org/10.1007/s00464-013-3305-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-013-3305-9

Keywords

Search

Navigation