Skip to main content
Log in

Routine near infra-red indocyanine green fluorescent cholangiography versus intraoperative cholangiography during laparoscopic cholecystectomy: a case-matched comparison

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

The aim is to evaluate safety and efficacy of near infra-red (NIR) indocyanine green (ICG) fluorescence structural imaging during laparoscopic cholecystectomy (LC) (Group A) and to compare perioperative data, including operative time, with a series of patients who underwent LC with routine traditional intraoperative cholangiography (IOC) (Group B).

Methods

Forty-four patients with acute or chronic cholecystitis underwent NIR-ICG fluorescent cholangiography during LC. ICG was administered intravenously at different time intervals or by direct gallbladder injection during surgery. Fluorescence intensity and anatomy identification were scored according to a visual analogue scale between 1 (least accurate) and 5 (most accurate). Group B patients (n = 44) were chosen from a prospectively maintained database of patients who underwent LC with routine IOC, matched for age, sex, body mass index, and diagnosis with group A patients.

Results

No adverse reactions were recorded. In group A, mean time between intravenous administration of ICG and surgery was 10.7 ± 8.2 (range 2–52) h. Administered doses ranged from 3.5 to 13.5 mg. Fluorescence was present in all cases, scoring ≥ 3 in 41 patients. Mean operative time was 86.9 ± 36.9 (30–180) min in group A and 117.9 ± 43.4 (40–220) min in group B (p = 0.0006). No conversion to open surgery nor bile duct injuries were observed in either group.

Conclusions

LC with NIR-ICG fluorescent cholangiography is safe and effective for early recognition of anatomical landmarks, reducing operative time as compared to LC with IOC, even when residents were the main operator. NIR-ICG fluorescent cholangiography was effective in patients with acute cholecystitis and in the obese. Data collection into large registries on the results of NIR-ICG fluorescent cholangiography during LC should be encouraged to establish whether this technique might set a new safety standard for LC.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Pucher PH, Brunt LM, Davies N, Linsk A, Munshi A, Rodriguez HA, Fingerhut A, Fanelli RD, Asbun H, Aggarwal R, SAGES Safe Cholecystectomy Task Force (2018) Outcome trends and safety measures after 30 years of laparoscopic cholecystectomy: a systematic review and pooled data analysis. Surg Endosc 32(5):2175–2183. https://doi.org/10.1007/s00464-017-5974-2

    Article  PubMed  PubMed Central  Google Scholar 

  2. National Center for Health Statistics. Health, United States, 2009. In Brief—medical technology (2010). https://www.cdc.gov/nchs/data/hus/hus09_InBrief_MedicalTech.pdf. Accessed 4 Jan 2019

  3. Flum DR, Dellinger EP, Cheadle A, Chan L, Koepsell T (2003) Intraoperative cholangiography and risk of common bile duct injury during cholecystectomy. JAMA 289(13):1639–1644

    Article  PubMed  Google Scholar 

  4. Gartland RM, Bloom JP, Fong ZV, DeRoo C, Dwyer K, Quinn G, Lillemoe K, Mort E (2018) What have we learned from malpractice claims involving the surgical management of benign biliary disease?: A 128 million dollar question. Ann Surg. https://doi.org/10.1097/sla.0000000000003155

    Article  Google Scholar 

  5. Harboe KM, Bardram L (2011) The quality of cholecystectomy in Denmark: outcome and risk factors for 20,307 patients from the national database. Surg Endosc 25(5):1630–1641. https://doi.org/10.1007/s00464-010-1453-8

    Article  PubMed  Google Scholar 

  6. Navez B, Ungureanu F, Michiels M, Claeys D, Muysoms F, Hubert C, Vanderveken M, Detry O, Detroz B, Closset J, Devos B, Kint M, Navez J, Zech F, Gigot JF, Belgian Group for Endoscopic Surgery (BGES) and the Hepatobiliary and Pancreatic Section (HBPS) of the Royal Belgian Society of Surgery (2012) Surgical management of acute cholecystitis: results of a 2-year prospective multicenter survey in Belgium. Surg Endosc 26(9):2436–2445

    Article  PubMed  Google Scholar 

  7. Törnqvist B, Strömberg C, Akre O, Enochsson L, Nilsson M (2015) Selective intraoperative cholangiography and risk of bile duct injury during cholecystectomy. Br J Surg 102(8):952–958. https://doi.org/10.1002/bjs.9832

    Article  PubMed  Google Scholar 

  8. Törnqvist B, Strömberg C, Persson G, Nilsson M (2012) Effect of intended intraoperative cholangiography and early detection of bile duct injury on survival after cholecystectomy: population based cohort study. BMJ 345:e6457. https://doi.org/10.1136/bmj.e6457

    Article  PubMed  PubMed Central  Google Scholar 

  9. Waage A, Nilsson M (2006) Iatrogenic bile duct injury: a population- based study of 152 776 cholecystectomies in the Swedish inpatient registry. Arch Surg 141(12):1207–1213

    Article  PubMed  Google Scholar 

  10. Dolan JP, Diggs BS, Sheppard BC, Hunter JG (2005) Ten-year trend in the national volume of bile duct injuries requiring operative repair. Surg Endosc 19(7):967–973

    Article  CAS  PubMed  Google Scholar 

  11. Landman MP, Feurer ID, Moore DE, Zaydfudim V, Pinson CW (2013) The long-term effect of bile duct injuries on health-related quality of life: a meta-analysis. HPB (Oxford) 15(4):252–259. https://doi.org/10.1111/j.1477-2574.2012.00586.x

    Article  Google Scholar 

  12. Fletcher DR, Hobbs MS, Tan P, Valinsky LJ, Hockey RL, Pikora TJ, Knuiman MW, Sheiner HJ, Edis A (1999) Complications of cholecystectomy: risks of the laparoscopic approach and protective effects of operative cholangiography: a population-based study. Ann Surg 229(4):449–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Fingerhut A, Dziri C, Garden OJ, Gouma D, Millat B, Neugebauer E, Paganini A, Targarona E (2013) ATOM, the all-inclusive, nominal EAES classification of bile duct injuries during cholecystectomy. Surg Endosc 27(12):4608–4619. https://doi.org/10.1007/s00464-013-3081-6

    Article  CAS  PubMed  Google Scholar 

  14. Rystedt JML, Tingstedt B, Montgomery F, Montgomery AK (2017) Routine intraoperative cholangiography during cholecystectomy is a cost-effective approach when analysing the cost of iatrogenic bile duct injuries. HPB (Oxford) 19(10):881–888. https://doi.org/10.1016/j.hpb.2017.06.004

    Article  Google Scholar 

  15. Dip FD, Asbun D, Rosales-Velderrain A, Lo Menzo E, Simpfendorfer CH, Szomstein S, Rosenthal RJ (2014) Cost analysis and effectiveness comparing the routine use of intraoperative fluorescent cholangiography with fluoroscopic cholangiogram in patients undergoing laparoscopic cholecystectomy. Surg Endosc 28(6):1838–1843. https://doi.org/10.1007/s00464-013-3394-5

    Article  PubMed  Google Scholar 

  16. Strasberg SM, Hertl M, Soper NJ (1995) An analysis of the problem of biliary injury during laparoscopic cholecystectomy. J Am Coll Surg 180(1):101–125

    CAS  PubMed  Google Scholar 

  17. Booij KA, de Reuver PR, Nijsse B, Busch OR, van Gulik TM, Gouma DJ (2014) Insufficient safety measures reported in operation notes of complicated laparoscopic cholecystectomies. Surgery 155(3):384–389. https://doi.org/10.1016/j.surg.2013.10.010.epub

    Article  PubMed  Google Scholar 

  18. Deal SB, Stefanidis D, Telem D, Fanelli RD, McDonald M, Ujiki M, Michael Brunt L, Alseidi AA (2017) Evaluation of crowd-sourced assessment of the critical view of safety in laparoscopic cholecystectomy. Surg Endosc 31(12):5094–5100. https://doi.org/10.1007/s00464-017-5574-1

    Article  PubMed  Google Scholar 

  19. Boni L, David G, Mangano A, Dionigi G, Rausei S, Spampatti S, Cassinotti E, Fingerhut A (2015) Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc 29(7):2046–2055. https://doi.org/10.1007/s00464-014-3895-x

    Article  PubMed  Google Scholar 

  20. van den Bos J, Schols RM, Luyer MD, van Dam RM, Vahrmeijer AL, Meijerink WJ, Gobardhan PD, van Dam GM, Bouvy ND, Stassen LP (2016) Near-infrared fluorescence cholangiography assisted laparoscopic cholecystectomy versus conventional laparoscopic cholecystectomy (FALCON trial): study protocol for a multicentre randomised controlled trial. BMJ Open 6(8):e011668. https://doi.org/10.1136/bmjopen-2016-011668

    Article  PubMed  PubMed Central  Google Scholar 

  21. Schols RM, Bouvy ND, van Dam RM, Masclee AA, Dejong CH, Stassen LP (2013) Combined vascular and biliary fluorescence imaging in laparoscopic cholecystectomy. Surg Endosc 27(12):4511–4517. https://doi.org/10.1007/s00464-013-3100-7

    Article  PubMed  Google Scholar 

  22. 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(9):1369–1377. https://doi.org/10.1002/bjs.7125

    Article  CAS  PubMed  Google Scholar 

  23. Daskalaki D, Fernandes E, Wang X, Bianco FM, Elli EF, Ayloo S, Masrur M, Milone L, Giulianotti PC (2014) Indocyanine green (ICG) fluorescent cholangiography during robotic cholecystectomy: results of 184 consecutive cases in a single institution. Surg Innov 21(6):615–621. https://doi.org/10.1177/1553350614524839

    Article  PubMed  Google Scholar 

  24. European Fluorescence Imaging-Guided Surgery (EURO-FIGS registry). http://www.euro-figs.eu. Accessed 16 Jan 2019

  25. Lezoche E, Paganini A, Guerrieri M, Carlei F, Lomanto D, Sottili M, Nardovino M (1994) Technique and results of routine dynamic cholangiography during 528 consecutive laparoscopic cholecystectomies. Surg Endosc 8(12):1443–1447

    Article  CAS  PubMed  Google Scholar 

  26. Graves C, Ely S, Idowu O, Newton C, Kim S (2017) Direct gallbladder indocyanine green injection fluorescence cholangiography during laparoscopic cholecystectomy. J Laparoendosc Adv Surg Tech A 27(10):1069–1073. https://doi.org/10.1089/lap.2017.0070

    Article  PubMed  Google Scholar 

  27. Quaresima S, Balla A, Guerrieri M, Campagnacci R, Lezoche E, Paganini AM (2017) A 23 year experience with laparoscopic common bile duct exploration. HPB (Oxford) 19(1):29–35. https://doi.org/10.1016/j.hpb.2016.10.011

    Article  Google Scholar 

  28. Quaresima S, Balla A, Guerrieri M, Lezoche G, Campagnacci R, D’Ambrosio G, Lezoche E, Paganini AM (2016) Results of medium seventeen years’ follow-up after laparoscopic choledochotomy for ductal stones. Gastroenterol Res Pract 2016:9506406. https://doi.org/10.1155/2016/9506406

    Article  PubMed  PubMed Central  Google Scholar 

  29. Takada T, Strasberg SM, Solomkin JS, Pitt HA, Gomi H, Yoshida M, Mayumi T, Miura F, Gouma DJ, Garden OJ, Büchler MW, Kiriyama S, Yokoe M, Kimura Y, Tsuyuguchi T, Itoi T, Gabata T, Higuchi R, Okamoto K, Hata J, Murata A, Kusachi S, Windsor JA, Supe AN, Lee S, Chen XP, Yamashita Y, Hirata K, Inui K, Sumiyama Y, Committee Tokyo Guidelines Revision (2013) TG13: Updated Tokyo Guidelines for the management of acute cholangitis and cholecystitis. J Hepatobiliary Pancreat Sci 20(1):1–7. https://doi.org/10.1007/s00534-012-0566-y

    Article  PubMed  Google Scholar 

  30. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibañes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M (2009) The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 250(2):187–196. https://doi.org/10.1097/SLA.0b013e3181b13ca2

    Article  PubMed  Google Scholar 

  31. Diana M, Soler L, Agnus V, D’Urso A, Vix M, Dallemagne B, Faucher V, Roy C, Mutter D, Marescaux J, Pessaux P (2017) Prospective evaluation of precision multimodal gallbladder surgery navigation: virtual reality, near-infrared fluorescence, and X-ray-based intraoperative cholangiography. Ann Surg 266(5):890–897. https://doi.org/10.1097/SLA.0000000000002400

    Article  PubMed  Google Scholar 

  32. Roy M, Dip F, Nguyen D, Simpfendorfer CH, Menzo EL, Szomstein S, Rosenthal RJ (2017) Fluorescent incisionless cholangiography as a teaching tool for identification of Calot’s triangle. Surg Endosc 31(6):2483–2490. https://doi.org/10.1007/s00464-016-5250-x

    Article  PubMed  Google Scholar 

  33. Way LW, Stewart L, Gantert W, Liu K, Lee CM, Whang K, Hunter JG (2003) Causes and prevention of laparoscopic bile duct injuries: analysis of 252 cases from a human factors and cognitive psychology perspective. Ann Surg 237(4):460–469

    PubMed  PubMed Central  Google Scholar 

  34. Ford JA, Soop M, Du J, Loveday BP, Rodgers M (2012) Systematic review of intraoperative cholangiography in cholecystectomy. Br J Surg 99(2):160–167. https://doi.org/10.1002/bjs.7809

    Article  CAS  PubMed  Google Scholar 

  35. Vlek SL, van Dam DA, Rubinstein SM, de Lange-de Klerk ESM, Schoonmade LJ, Tuynman JB, Meijerink WJHJ, Ankersmit M (2017) Biliary tract visualization using near-infrared imaging with indocyanine green during laparoscopic cholecystectomy: results of a systematic review. Surg Endosc 31(7):2731–2742. https://doi.org/10.1007/s00464-016-5318-7

    Article  CAS  PubMed  Google Scholar 

  36. Zroback C, Chow G, Meneghetti A, Warnock G, Meloche M, Chiu CJ, Panton ON (2016) Fluorescent cholangiography in laparoscopic cholecystectomy: the initial Canadian experience. Am J Surg 211(5):933–937. https://doi.org/10.1016/j.amjsurg.2016.01.013

    Article  PubMed  Google Scholar 

  37. Dip F, LoMenzo E, Sarotto L, Phillips E, Todeschini H, Nahmod M, Alle L, Schneider S, Kaja L, Boni L, Ferraina P, Carus T, Kokudo N, Ishizawa T, Walsh M, Simpfendorfer C, Mayank R, White K, Rosenthal RJ (2019) Randomized trial of near-infrared incisionless fluorescent cholangiography. Ann Surg. https://doi.org/10.1097/sla.0000000000003178

    Article  PubMed  Google Scholar 

  38. Millat B, Atger J, Deleuze A, Briandet H, Fingerhut A, Guillon F, Marrel E, De Seguin C, Soulier P (1997) Laparoscopic treatment for choledocholithiasis: a prospective evaluation in 247 consecutive unselected patients. Hepatogastroenterology 44(13):28–34

    CAS  PubMed  Google Scholar 

  39. Tranter SE, Thompson MH (2003) A prospective single-blinded controlled study comparing laparoscopic ultrasound of the common bile duct with operative cholangiography. Surg Endosc 17(2):216–219

    Article  CAS  PubMed  Google Scholar 

  40. Dili A, Bertrand C (2017) Laparoscopic ultrasonography as an alternative to intraoperative cholangiography during laparoscopic cholecystectomy. World J Gastroenterol 23(29):5438–5450. https://doi.org/10.3748/wjg.v23.i29.5438

    Article  PubMed  PubMed Central  Google Scholar 

  41. Eikermann M, Siegel R, Broeders I, Dziri C, Fingerhut A, Gutt C, Jaschinski T, Nassar A, Paganini AM, Pieper D, Targarona E, Schrewe M, Shamiyeh A, Strik M, Neugebauer EA, European Association for Endoscopic Surgery (2012) Prevention and treatment of bile duct injuries during laparoscopic cholecystectomy: the clinical practice guidelines of the European Association for Endoscopic Surgery (EAES). Surg Endosc 26(11):3003–3039. https://doi.org/10.1007/s00464-012-2511-1

    Article  CAS  PubMed  Google Scholar 

  42. Pucher PH, Brunt LM, Fanelli RD, Asbun HJ, Aggarwal R (2015) SAGES expert Delphi consensus: critical factors for safe surgical practice in laparoscopic cholecystectomy. Surg Endosc 29(11):3074–3085. https://doi.org/10.1007/s00464-015-4079-z

    Article  PubMed  Google Scholar 

  43. Balla A, Quaresima S, Corona M, Lucatelli P, Fiocca F, Rossi M, Bezzi M, Catalano C, Salvatori FM, Fingerhut A, Paganini AM (2018) ATOM classification of bile duct injuries during laparoscopic cholecystectomy: analysis of a single institution experience. J Laparoendosc Adv Surg Tech A. https://doi.org/10.1089/lap.2018.0413

    Article  PubMed  Google Scholar 

  44. Strasberg SM, Brunt LM (2017) The critical view of safety: why it is not the only method of ductal identification within the standard of care in laparoscopic cholecystectomy. Ann Surg 265(3):464–465. https://doi.org/10.1097/SLA.0000000000002054

    Article  PubMed  Google Scholar 

  45. Kawaguchi Y, Ishizawa T, Miyata Y, Yamashita S, Masuda K, Satou S, Tamura S, Kaneko J, Sakamoto Y, Aoki T, Hasegawa K, Sugawara Y, Kokudo N (2013) Portal uptake function in veno-occlusive regions evaluated by real-time fluorescent imaging using indocyanine green. J Hepatol 58(2):247–253. https://doi.org/10.1016/j.jhep.2012.09.028

    Article  PubMed  Google Scholar 

  46. Verbeek FP, Schaafsma BE, Tummers QR, van der Vorst JR, van der Made WJ, Baeten CI, Bonsing BA, Frangioni JV, van de Velde CJ, Vahrmeijer AL, Swijnenburg RJ (2014) Optimization of near-infrared fluorescence cholangiography for open and laparoscopic surgery. Surg Endosc 28(4):1076–1082

    Article  PubMed  PubMed Central  Google Scholar 

  47. Gutt CN, Encke J, Köninger J, Harnoss JC, Weigand K, Kipfmüller K, Schunter O, Götze T, Golling MT, Menges M, Klar E, Feilhauer K, Zoller WG, Ridwelski K, Ackmann S, Baron A, Schön MR, Seitz HK, Daniel D, Stremmel W, Büchler MW (2013) Acute cholecystitis: early versus delayed cholecystectomy, a multicenter randomized trial (ACDCstudy, NCT00447304). Ann Surg 258(3):385–393. https://doi.org/10.1097/SLA.0b013e3182a1599b

    Article  PubMed  Google Scholar 

  48. Boni L, Cassinotti EC, David G, Marzorati AM, Fingerhut A (2015) Indocyanine green-enhanced fluorescence cholangiography in laparoscopic cholecystectomy: experience from 100 cases. J Am Coll Surg 221(4):S71

    Article  Google Scholar 

  49. Osayi SN, Wendling MR, Drosdeck JM, Chaudhry UI, Perry KA, Noria SF, Mikami DJ, Needleman BJ, Muscarella P 2nd, Abdel-Rasoul M, Renton DB, Melvin WS, Hazey JW, Narula VK (2015) Nera-infrared fluorescent cholangiography facilitates identification of biliary anatomy during laparoscopic cholecystectomy. Surg Endosc 29(2):368–375. https://doi.org/10.1007/s00464-014-3677-5

    Article  PubMed  Google Scholar 

  50. Dip F, Nguyen D, Montorfano L, Szretter Noste ME, Lo Menzo E, Simpfendorfer C, Szomstein S, Rosenthal R (2016) Accuracy of near infrared-guided surgery in morbidly obese subjects undergiong laparoscopic cholecystectomy. Obes Surg 26(3):525–530. https://doi.org/10.1007/s11695-015-1781-9

    Article  PubMed  Google Scholar 

  51. Liu YY, Kong SH, Diana M, Lègner A, Wu CC, Kameyama N, Dallemagne B, Marescaux J (2016) Near-infrared cholecysto-cholangiography with indocyanine green may secure cholecystectomy in difficult clinical situations: proof of the concept in a porcine model. Surg Endosc 30(9):4115–4123. https://doi.org/10.1007/s00464-015-4608-9

    Article  PubMed  Google Scholar 

  52. Ankersmit M, van Dam DA, van Rijswijk AS, van den Heuvel B, Tuynman JB, Meijerink WJHJ (2017) Fluorescent imaging with indocyanine green during laparoscopic cholecystectomy in patients at increased risk of bile duct injury. Surg Innov 24(3):245–252. https://doi.org/10.1177/1553350617690309

    Article  PubMed  PubMed Central  Google Scholar 

  53. Bergamaschi R, Ignjatovic D (2000) More than two structures in Calot’s triangle. A postmortem study. Surg Endosc 14(4):354–357

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Silvia Quaresima.

Ethics declarations

Disclosures

Silvia Quaresima, Andrea Balla, Livia Palmieri, Ardit Seitaj, Abe Fingerhut, Pietro Ursi, and Alessandro M. Paganini declare that they have no conflicts of interest or financial ties to disclose.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Quaresima, S., Balla, A., Palmieri, L. et al. Routine near infra-red indocyanine green fluorescent cholangiography versus intraoperative cholangiography during laparoscopic cholecystectomy: a case-matched comparison. Surg Endosc 34, 1959–1967 (2020). https://doi.org/10.1007/s00464-019-06970-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-019-06970-0

Keywords

Navigation