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Best practices in near-infrared fluorescence imaging with indocyanine green (NIRF/ICG)-guided robotic urologic surgery: a systematic review-based expert consensus

  • Giovanni E. CacciamaniEmail author
  • A. Shakir
  • A. Tafuri
  • K. Gill
  • J. Han
  • N. Ahmadi
  • P. A. Hueber
  • M. Gallucci
  • G. Simone
  • R. Campi
  • G. Vignolini
  • W. C. Huang
  • J. Taylor
  • E. Becher
  • F. W. B. Van Leeuwen
  • H. G. Van Der Poel
  • L. P. Velet
  • A. K. Hemal
  • A. Breda
  • R. Autorino
  • R. Sotelo
  • M. Aron
  • M. M. Desai
  • A. L. De Castro Abreu
Topic Paper

Abstract

Purpose

The aim of the present study is to investigate the impact of the near-infrared (NIRF) technology with indocyanine green (ICG) in robotic urologic surgery by performing a systematic literature review and to provide evidence-based expert recommendations on best practices in this field.

Methods

All English language publications on NIRF/ICG-guided robotic urologic procedures were evaluated. We followed the PRISMA (Preferred Reporting Items for Systematic Review and Meta-Analyses) statement to evaluate PubMed®, Scopus® and Web of Science™ databases (up to April 2019). Experts in the field provided detailed pictures and intraoperative video-clips of different NIRF/ICG-guided robotic surgeries with recommendations for each procedure. A unique QRcode was generated and linked to each underlying video-clip. This new exclusive feature makes the present the first “dynamic paper” that merges text and figure description with their own video providing readers an innovative, immersive, high-quality and user-friendly experience.

Results

Our electronic search identified a total of 576 papers. Of these, 36 studies included in the present systematic review reporting the use of NIRF/ICG in robotic partial nephrectomy (n = 13), robotic radical prostatectomy and lymphadenectomy (n = 7), robotic ureteral re-implantation and reconstruction (n = 5), robotic adrenalectomy (n = 4), robotic radical cystectomy (n = 3), penectomy and robotic inguinal lymphadenectomy (n = 2), robotic simple prostatectomy (n = 1), robotic kidney transplantation (n = 1) and robotic sacrocolpopexy (n = 1).

Conclusion

NIRF/ICG technology has now emerged as a safe, feasible and useful tool that may facilitate urologic robotic surgery. It has been shown to improve the identification of key anatomical landmarks and pathological structures for oncological and non-oncological procedures. Level of evidence is predominantly low. Larger series with longer follow-up are needed, especially in assessing the quality of the nodal dissection and the feasibility of the identification of sentinel nodes and the impact of these novel technologies on long-term oncological and functional outcomes.

Keywords

ICG Indocyanine green NIRF Near-infrared fluorescence Firefly: robotic surgery Urology Robotic partial nephrectomy Robotic adrenalectomy Robotic radical prostatectomy Lymphadenectomy Robotic radical cystectomy 

Notes

Author contributions

Protocol/project development: GEC, AS, AT. Data collection or management: GEC, AS, AT, KG, JH. Data analysis: GEC, AS, AT. Manuscript writing/editing: GEC, AS, AT, NA, PAH, MG, GS, RC, GV, WCH, JT, EB, FWBL, HGP, LPV, AKH, AB, RA, RS, MA, MMD, ALCA.

Compliance with ethical standards

Conflict of interest

Disclosures Dr. Mihir Desai is a consultant for Auris Robotics and PROCEPT BioRobotics. Dr. Monish Aron is a consultant for Intuitive Surgical.

Informed consent

The study complied with the Declaration of Helsinki. All patients provided written informed consent prior to their surgical procedure.

Supplementary material

345_2019_2870_MOESM1_ESM.docx (25 kb)
Supplementary material 1 (DOCX 25 kb)

References

  1. 1.
    Nair R, Aggarwal R, Khanna D (2011) Methods of formal consensus in classification/diagnostic criteria and guideline development. Semin Arthritis Rheum 41(2):95–105Google Scholar
  2. 2.
    Reinhart MB, Huntington CR, Blair LJ, Heniford BT, Augenstein VA (2016) Indocyanine green: historical context, current applications, and future considerations. Surg Innov 23(2):166–175Google Scholar
  3. 3.
    Veccia A, Antonelli A, Hampton LJ, Greco F, Perdona S, Lima E et al (2019) Near-infrared fluorescence imaging with indocyanine green in robot-assisted partial nephrectomy: pooled analysis of comparative studies. Eur Urol Focus.  https://doi.org/10.1016/j.euf.2019.03.005 Google Scholar
  4. 4.
    Huang SW, Ou JJ, Wong HP (2018) The use of indocyanine green imaging technique in patient with hepatocellular carcinoma. Transl Gastroenterol Hepatol 3:95Google Scholar
  5. 5.
    Newton AD, Predina JD (2018) Intraoperative fluorescence imaging in thoracic surgery. J Surg Oncol 118(2):344–355Google Scholar
  6. 6.
    Nie S, Low PS, Singhal S, Mangano A, Masrur MA, Bustos R et al (2018) Near-infrared indocyanine green-enhanced fluorescence and minimally invasive colorectal surgery: review of the literature. J Surg Oncol 33:77–83Google Scholar
  7. 7.
    Spinoglio G, Bertani E, Borin S, Piccioli A, Petz W (2018) Green indocyanine fluorescence in robotic abdominal surgery. Updates Surg 70(3):375–379Google Scholar
  8. 8.
    Tobis S, Knopf J, Silvers C, Yao J, Rashid H, Wu G et al (2011) Near infrared fluorescence imaging with robotic assisted laparoscopic partial nephrectomy: initial clinical experience for renal cortical tumors. J Urol 186(1):47–52Google Scholar
  9. 9.
    Basile G, Breda A, Gomez Rivas J, Cacciamani G, Okhunov Z, Dourado A et al (2019) Comparison between near-infrared fluorescence imaging with indocyanine green and InfraRed imaging: on-bench trial for kidney perfusion analysis. A project by ESUT-YAUWP group. Minerva Urol Nefrol 71(3):280–285.  https://doi.org/10.23736/S0393-2249.19.03353-8 Google Scholar
  10. 10.
    Autorino R, Zargar H, White WM, Novara G, Annino F, Perdona S et al (2014) Current applications of near-infrared fluorescence imaging in robotic urologic surgery: a systematic review and critical analysis of the literature. Urology 84(4):751–759Google Scholar
  11. 11.
    Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6(7):e1000097Google Scholar
  12. 12.
    Howick J, Chalmers I, Glasziou P, Greenhalgh T, Heneghan C, Liberati A, Moschetti I, Phillips B, Thornton H (2016) Explanation of the 2011 Oxford Centre for Evidence-Based Medicine (OCEBM) Levels of Evidence (Background Document). Oxford Centre for Evidence-Based Medicine. http://www.cebm.net/index.aspx?o=5653. Accessed 01 Jan 2019
  13. 13.
    Krane LS, Manny TB, Hemal AK (2012) Is near infrared fluorescence imaging using indocyanine green dye useful in robotic partial nephrectomy: a prospective comparative study of 94 patients. Urology 80(1):110–116Google Scholar
  14. 14.
    Tobis S, Knopf JK, Silvers C, Messing E, Yao J, Rashid H et al (2012) Robot-assisted and laparoscopic partial nephrectomy with near infrared fluorescence imaging. J Endourol 26(7):797–802Google Scholar
  15. 15.
    Angell JE, Khemees TA, Abaza R (2013) Optimization of near infrared fluorescence tumor localization during robotic partial nephrectomy. J Urol 190(5):1668–1673Google Scholar
  16. 16.
    Borofsky MS, Gill IS, Hemal AK, Marien TP, Jayaratna I, Krane LS et al (2013) Near-infrared fluorescence imaging to facilitate super-selective arterial clamping during zero-ischaemia robotic partial nephrectomy. BJU Int 111(4):604–610Google Scholar
  17. 17.
    Manny TB, Krane LS, Hemal AK (2013) Indocyanine green cannot predict malignancy in partial nephrectomy: histopathologic correlation with fluorescence pattern in 100 patients. J Endourol 27(7):918–921Google Scholar
  18. 18.
    Harke N, Schoen G, Schiefelbein F, Heinrich E (2014) Selective clamping under the usage of near-infrared fluorescence imaging with indocyanine green in robot-assisted partial nephrectomy: a single-surgeon matched-pair study. World J Urol 32(5):1259–1265Google Scholar
  19. 19.
    McClintock TR, Bjurlin MA, Wysock JS, Borofsky MS, Marien TP, Okoro C et al (2014) Can selective arterial clamping with fluorescence imaging preserve kidney function during robotic partial nephrectomy? Urology 84(2):327–332Google Scholar
  20. 20.
    Bjurlin MA, McClintock TR, Stifelman MD (2015) Near-infrared fluorescence imaging with intraoperative administration of indocyanine green for robotic partial nephrectomy. Curr Urol Rep 16(4):20Google Scholar
  21. 21.
    Dominique I, Paparel P (2016) Indications and technique of intraveinous indocyanine green-based fluorescence during robotic-assisted partial nephrectomy. Prog Urol FMC 26(4):F76–F79Google Scholar
  22. 22.
    Herz D, DaJusta D, Ching C, McLeod D (2016) Segmental arterial mapping during pediatric robot-assisted laparoscopic heminephrectomy: a descriptive series. J Pediatr Urol 12(4):266.e1–266.e6Google Scholar
  23. 23.
    Arora S, Rogers C (2018) Partial nephrectomy in central renal tumors. J Endourol 32(S1):S63–S67Google Scholar
  24. 24.
    Lanchon C, Arnoux V, Fiard G, Descotes JL, Rambeaud JJ, Lefrancq JB et al (2018) Super-selective robot-assisted partial nephrectomy using near-infrared fluorescence versus early-unclamping of the renal artery: results of a prospective matched-pair analysis. Int Braz J Urol 44(1):53–62Google Scholar
  25. 25.
    Mattevi D, Luciani LG, Mantovani W, Cai T, Chiodini S, Vattovani V et al (2019) Fluorescence-guided selective arterial clamping during RAPN provides better early functional outcomes based on renal scan compared to standard clamping. J Robot Surg 13:391–396Google Scholar
  26. 26.
    Simone G, Tuderti G, Anceschi U, Ferriero M, Costantini M, Minisola F et al (2019) “Ride the green light”: indocyanine green-marked off-clamp robotic partial nephrectomy for totally endophytic renal masses. Eur Urol 75:1008–1014Google Scholar
  27. 27.
    Bjurlin MA, Gan M, McClintock TR, Volpe A, Borofsky MS, Mottrie A et al (2014) Near-infrared fluorescence imaging: emerging applications in robotic upper urinary tract surgery. Eur Urol 65(4):793–801Google Scholar
  28. 28.
    Mitsui Y, Shiina H, Arichi N, Hiraoka T, Inoue S, Sumura M et al (2012) Indocyanine green (ICG)-based fluorescence navigation system for discrimination of kidney cancer from normal parenchyma: application during partial nephrectomy. Int Urol Nephrol 44(3):753–759Google Scholar
  29. 29.
    Mangano MS, De Gobbi A, Beniamin F, Lamon C, Ciaccia M, Maccatrozzo L (2018) Robot-assisted nerve-sparing radical prostatectomy using near-infrared fluorescence technology and indocyanine green: initial experience. Urologia 85(1):29–31Google Scholar
  30. 30.
    van der Poel HG, Buckle T, Brouwer OR, Valdes Olmos RA, van Leeuwen FW (2011) Intraoperative laparoscopic fluorescence guidance to the sentinel lymph node in prostate cancer patients: clinical proof of concept of an integrated functional imaging approach using a multimodal tracer. Eur Urol 60(4):826–833Google Scholar
  31. 31.
    KleinJan GH, van den Berg NS, Brouwer OR, de Jong J, Acar C, Wit EM et al (2014) Optimisation of fluorescence guidance during robot-assisted laparoscopic sentinel node biopsy for prostate cancer. Eur Urol 66(6):991–998Google Scholar
  32. 32.
    KleinJan GH, van den Berg NS, de Jong J, Wit EM, Thygessen H, Vegt E et al (2016) Multimodal hybrid imaging agents for sentinel node mapping as a means to (re)connect nuclear medicine to advances made in robot-assisted surgery. Eur J Nucl Med Mol Imaging 43(7):1278–1287Google Scholar
  33. 33.
    Chennamsetty A, Zhumkhawala A, Tobis SB, Ruel N, Lau CS, Yamzon J et al (2017) Lymph node fluorescence during robot-assisted radical prostatectomy with indocyanine green: prospective dosing analysis. Clin Genitourin Cancer 15(4):e529–e534Google Scholar
  34. 34.
    van den Berg NS, Buckle T, KleinJan GH, van der Poel HG, van Leeuwen FWB (2017) Multispectral fluorescence imaging during robot-assisted laparoscopic sentinel node biopsy: a first step towards a fluorescence-based anatomic roadmap. Eur Urol 72(1):110–117Google Scholar
  35. 35.
    Harke NN, Godes M, Wagner C, Addali M, Fangmeyer B, Urbanova K et al (2018) Fluorescence-supported lymphography and extended pelvic lymph node dissection in robot-assisted radical prostatectomy: a prospective, randomized trial. World J Urol 36(11):1817–1823Google Scholar
  36. 36.
    Lee Z, Simhan J, Parker DC, Reilly C, Llukani E, Lee DI et al (2013) Novel use of indocyanine green for intraoperative, real-time localization of ureteral stenosis during robot-assisted ureteroureterostomy. Urology 82(3):729–733Google Scholar
  37. 37.
    Siddighi S, Yune JJ, Hardesty J (2014) Indocyanine green for intraoperative localization of ureter. Am J Obstet Gynecol 211(4):436.e1–436.e2Google Scholar
  38. 38.
    Lee Z, Moore B, Giusto L, Eun DD (2015) Use of indocyanine green during robot-assisted ureteral reconstructions. Eur Urol 67(2):291–298Google Scholar
  39. 39.
    Lee Z, Sterling ME, Keehn AY, Lee M, Metro MJ, Eun DD (2019) The use of indocyanine green during robotic ureteroenteric reimplantation for the management of benign anastomotic strictures. World J Urol 37:1211–1216Google Scholar
  40. 40.
    Manny TB, Pompeo AS, Hemal AK (2013) Robotic partial adrenalectomy using indocyanine green dye with near-infrared imaging: the initial clinical experience. Urology 82(3):738–742Google Scholar
  41. 41.
    Colvin J, Zaidi N, Berber E (2016) The utility of indocyanine green fluorescence imaging during robotic adrenalectomy. J Surg Oncol 114(2):153–156Google Scholar
  42. 42.
    Sound S, Okoh AK, Bucak E, Yigitbas H, Dural C, Berber E (2016) Intraoperative tumor localization and tissue distinction during robotic adrenalectomy using indocyanine green fluorescence imaging: a feasibility study. Surg Endosc 30(2):657–662Google Scholar
  43. 43.
    Kahramangil B, Kose E, Berber E (2018) Characterization of fluorescence patterns exhibited by different adrenal tumors: determining the indications for indocyanine green use in adrenalectomy. Surgery 164(5):972–977Google Scholar
  44. 44.
    Manny TB, Hemal AK (2014) Fluorescence-enhanced robotic radical cystectomy using unconjugated indocyanine green for pelvic lymphangiography, tumor marking, and mesenteric angiography: the initial clinical experience. Urology 83(4):824–829Google Scholar
  45. 45.
    Chopra S, de Castro Abreu AL, Berger AK, Sehgal S, Gill I, Aron M et al (2017) Evolution of robot-assisted orthotopic ileal neobladder formation: a step-by-step update to the University of Southern California (USC) technique. BJU Int 119(1):185–191Google Scholar
  46. 46.
    Ahmadi N, Ashrafi AN (2019) Use of indocyanine green to minimise uretero-enteric strictures after robotic radical cystectomy. BJU Int.  https://doi.org/10.1111/bju.14733 Google Scholar
  47. 47.
    Bjurlin MA, Zhao LC, Kenigsberg AP, Mass AY, Taneja SS, Huang WC (2017) Novel use of fluorescence lymphangiography during robotic groin dissection for penile cancer. Urology 107:267Google Scholar
  48. 48.
    Savio LF, Panizzutti Barboza M, Alameddine M, Ahdoot M, Alonzo D, Ritch CR (2018) Combined partial penectomy with bilateral robotic inguinal lymphadenectomy using near-infrared fluorescence guidance. Urology 113:251Google Scholar
  49. 49.
    Simone G, Misuraca L, Anceschi U, Minisola F, Ferriero M, Guaglianone S et al (2019) Urethra and ejaculation preserving robot-assisted simple prostatectomy: near-infrared fluorescence imaging-guided Madigan technique. Eur Urol 75(3):492–497Google Scholar
  50. 50.
    Vignolini G, Sessa F, Greco I, Cito G, Vanacore D, Cocci A et al (2019) Intraoperative assessment of ureteral and graft reperfusion during robotic kidney transplantation with indocyanine green fluorescence videography. Minerv Urol Nefrol 71(1):79–84Google Scholar
  51. 51.
    Xia L, Zeh R, Mizelle J, Newton A, Predina J, Nie S et al (2017) Near-infrared intraoperative molecular imaging can identify metastatic lymph nodes in prostate cancer. Urology 106:133–138Google Scholar
  52. 52.
    Meershoek P, KleinJan GH, van Oosterom MN, Wit EMK, van Willigen DM, Bauwens KP et al (2018) Multispectral-fluorescence imaging as a tool to separate healthy from disease-related lymphatic anatomy during robot-assisted laparoscopy. J Nucl Med 59(11):1757–1760Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Giovanni E. Cacciamani
    • 1
    Email author
  • A. Shakir
    • 1
  • A. Tafuri
    • 1
    • 2
  • K. Gill
    • 1
  • J. Han
    • 1
  • N. Ahmadi
    • 1
    • 3
  • P. A. Hueber
    • 1
  • M. Gallucci
    • 4
  • G. Simone
    • 4
  • R. Campi
    • 5
    • 6
  • G. Vignolini
    • 5
    • 6
  • W. C. Huang
    • 7
  • J. Taylor
    • 7
  • E. Becher
    • 7
  • F. W. B. Van Leeuwen
    • 8
    • 9
    • 10
  • H. G. Van Der Poel
    • 8
  • L. P. Velet
    • 11
  • A. K. Hemal
    • 11
  • A. Breda
    • 12
  • R. Autorino
    • 13
  • R. Sotelo
    • 1
  • M. Aron
    • 1
  • M. M. Desai
    • 1
  • A. L. De Castro Abreu
    • 1
  1. 1.USC Institute of Urology and Catherine and Joseph Aresty Department of Urology, Keck School of MedicineUniversity of Southern CaliforniaLos AngelesUSA
  2. 2.Department of UrologyUniversity of VeronaVeronaItaly
  3. 3.Department of Uro-OncologyChris O’Brien LifehouseCamperdownAustralia
  4. 4.Department of Urology“Regina Elena” National Cancer InstituteRomeItaly
  5. 5.Department of Urologic Robotic Surgery and Renal Transplantation, Careggi HospitalUniversity of FlorenceFlorenceItaly
  6. 6.Department of Experimental and Clinical MedicineUniversity of FlorenceFlorenceItaly
  7. 7.Division of Urologic Oncology, Department of UrologyNYU Langone HealthNew YorkUSA
  8. 8.Department of UrologyAntoni van Leeuwenhoek Hospital, Netherlands Cancer InstituteAmsterdamThe Netherlands
  9. 9.Interventional Molecular Imaging LaboratoryLeiden University Medical centerLeidenThe Netherlands
  10. 10.Orsi AcademyMelleBelgium
  11. 11.Department of UrologyWake Forest UniversityWinston-SalemUSA
  12. 12.Fundació Puigvert, Department of UrologyAutonomous University of BarcelonaBarcelonaSpain
  13. 13.Division of Urology, Department of SurgeryVCU HealthRichmondUSA

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