Skip to main content

Advertisement

SpringerLink
Log in

Computer-assisted quantification and visualization of bowel perfusion using fluorescence-based enhanced reality in left-sided colonic resections

  • Published:
Surgical Endoscopy Aims and scope Submit manuscript

Abstract

Background

Fluorescence-based enhanced reality (FLER) is a computer-based quantification method of fluorescence angiographies to evaluate bowel perfusion. The aim of this prospective trial was to assess the clinical feasibility and to correlate FLER with metabolic markers of perfusion, during colorectal resections.

Methods

FLER analysis and visualization was performed in 22 patients (diverticulitis n = 17; colorectal cancer n = 5) intra- and extra-abdominally during distal and proximal resection, respectively. The fluorescence signal of indocyanine green (0.2 mg/kg) was captured using a near-infrared camera and computed to create a virtual color-coded cartography. This was overlaid onto the bowel (enhanced reality). It helped to identify regions of interest (ROIs) where samples were subsequently obtained. Resections were performed strictly guided according to clinical decision. On the surgical specimen, samplings were made at different ROIs to measure intestinal lactates (mmol/L) and mitochondria efficiency as acceptor control ratio (ACR).

Results

The native (unquantified) fluorescent signal diffused to obvious ischemic areas during the distal appreciation. Proximally, a lower diffusion of ICG was observed. Five anastomotic complications occurred. The expected values of local capillary lactates were correlated with the measured values both proximally (3.62 ± 2.48 expected vs. 3.17 ± 2.8 actual; rho 0.89; p = 0.0006) and distally (4.5 ± 3 expected vs. 4 ± 2.5 actual; rho 0.73; p = 0.0021). FLER values correlated with ACR at the proximal site (rho 0.76; p = 0.04) and at the ischemic zone (rho 0.71; p = 0.01). In complicated cases, lactates at the proximal resection site were higher (5.8 ± 4.5) as opposed to uncomplicated cases (2.45 ± 1.5; p = 0.008). ACR was reduced proximally in complicated (1.3 ± 0.18) vs. uncomplicated cases (1.68 ± 0.3; p = 0.023).

Conclusions

FLER allows to image the quantified fluorescence signal in augmented reality and provides a reproducible estimation of bowel perfusion (NCT02626091).

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
Fig. 5

Similar content being viewed by others

References

  1. Blanco-Colino R, Espin-Basany E (2018) Intraoperative use of ICG fluorescence imaging to reduce the risk of anastomotic leakage in colorectal surgery: a systematic review and meta-analysis. Tech Coloproctol 22(1):15–23

    Article  CAS  Google Scholar 

  2. Baiocchi GL, Diana M, Boni L (2018) Indocyanine green-based fluorescence imaging in visceral and hepatobiliary and pancreatic surgery: state of the art and future directions. World J Gastroenterol 24(27):2921–2930

    Article  Google Scholar 

  3. van Manen L, Handgraaf HJM, Diana M et al (2018) A practical guide for the use of indocyanine green and methylene blue in fluorescence-guided abdominal surgery. J Surg Oncol 118(2):283–300

    Article  Google Scholar 

  4. Jafari MD, Wexner SD, Martz JE et al (2015) Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR II): a multi-institutional study. J Am Coll Surg 220(1):82–92

    Article  Google Scholar 

  5. Ris F, Liot E, Buchs NC et al (2018) Multicentre phase II trial of near-infrared imaging in elective colorectal surgery. Br J Surg 105(10):1359–1367

    Article  CAS  Google Scholar 

  6. Kudszus S, Roesel C, Schachtrupp A et al (2010) Intraoperative laser fluorescence angiography in colorectal surgery: a noninvasive analysis to reduce the rate of anastomotic leakage. Langenbecks Arch Surg 395(8):1025–1030

    Article  Google Scholar 

  7. Kim JC, Lee JL, Yoon YS et al (2016) Utility of indocyanine-green fluorescent imaging during robot-assisted sphincter-saving surgery on rectal cancer patients. Int J Med Robot 12(4):710–717

    Article  Google Scholar 

  8. Kin C, Vo H, Welton L et al (2015) Equivocal effect of intraoperative fluorescence angiography on colorectal anastomotic leaks. Dis Colon Rectum 58(6):582–587

    Article  Google Scholar 

  9. Jafari MD, Lee KH, Halabi WJ et al (2013) The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc 27(8):3003–3008

    Article  Google Scholar 

  10. Boni L, Fingerhut A, Marzorati A et al (2017) Indocyanine green fluorescence angiography during laparoscopic low anterior resection: results of a case-matched study. Surg Endosc 31(4):1836–1840

    Article  Google Scholar 

  11. De Nardi P, Elmore U, Maggi G et al (2019) Intraoperative angiography with indocyanine green to assess anastomosis perfusion in patients undergoing laparoscopic colorectal resection: results of a multicenter randomized controlled trial. Surg Endosc 34(1):53–60

    Article  Google Scholar 

  12. van den Bos J, Al-Taher M, Schols RM et al (2018) Near-infrared fluorescence imaging for real-time intraoperative guidance in anastomotic colorectal surgery: a systematic review of literature. J Laparoendosc Adv Surg Tech A 28(2):157–167

    Article  Google Scholar 

  13. Wada T, Kawada K, Takahashi R et al (2017) ICG fluorescence imaging for quantitative evaluation of colonic perfusion in laparoscopic colorectal surgery. Surg Endosc 31(10):4184–4193

    Article  Google Scholar 

  14. Son GM, Kwon MS, Kim Y et al (2019) Quantitative analysis of colon perfusion pattern using indocyanine green (ICG) angiography in laparoscopic colorectal surgery. Surg Endosc 33(5):1640–1649

    Article  Google Scholar 

  15. Nerup N, Andersen HS, Ambrus R et al (2017) Quantification of fluorescence angiography in a porcine model. Langenbecks Arch Surg 402(4):655–662

    Article  Google Scholar 

  16. Diana M, Noll E, Agnus V et al (2017) Reply to letter: "Enhanced reality fluorescence videography to assess bowel perfusion: the cybernetic eye". Ann Surg 265(4):e49–e52

    Article  Google Scholar 

  17. Diana M, Noll E, Diemunsch P et al (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259(4):700–707

    Article  Google Scholar 

  18. Watanabe J, Ishibe A, Suwa Y et al (2019) Indocyanine green fluorescence imaging to reduce the risk of anastomotic leakage in laparoscopic low anterior resection for rectal cancer: a propensity score-matched cohort study. Surg Endosc 34(1):202–208

    Article  Google Scholar 

  19. Diana M (2017) Enabling precision digestive surgery with fluorescence imaging. Transl Gastroenterol Hepatol 2:97

    Article  Google Scholar 

  20. Mascagni P, Longo F, Barberio M et al (2018) New intraoperative imaging technologies: innovating the surgeon's eye toward surgical precision. J Surg Oncol 118(2):265–282

    Article  Google Scholar 

  21. Diana M, Halvax P, Dallemagne B et al (2014) Real-time navigation by fluorescence-based enhanced reality for precise estimation of future anastomotic site in digestive surgery. Surg Endosc 28(11):3108–3118

    Article  Google Scholar 

  22. Diana M, Dallemagne B, Chung H et al (2014) Probe-based confocal laser endomicroscopy and fluorescence-based enhanced reality for real-time assessment of intestinal microcirculation in a porcine model of sigmoid ischemia. Surg Endosc 28(11):3224–3233

    Article  Google Scholar 

  23. Diana M, Agnus V, Halvax P et al (2015) Intraoperative fluorescence-based enhanced reality laparoscopic real-time imaging to assess bowel perfusion at the anastomotic site in an experimental model. Br J Surg 102(2):e169–e176

    Article  CAS  Google Scholar 

  24. Quero G, Lapergola A, Barberio M et al (2019) Discrimination between arterial and venous bowel ischemia by computer-assisted analysis of the fluorescent signal. Surg Endosc 33(6):1988–1997

    Article  Google Scholar 

  25. Gosvig K, Jensen SS, Qvist N et al (2019) Remote computer-assisted analysis of ICG fluorescence signal for evaluation of small intestinal anastomotic perfusion: a blinded, randomized, experimental trial. Surg Endosc 34(5):2095–2102

    Article  Google Scholar 

  26. Seeliger B, Agnus V, Mascagni P et al (2019) Simultaneous computer-assisted assessment of mucosal and serosal perfusion in a model of segmental colonic ischemia. Surg Endosc. https://doi.org/10.1007/s00464-019-07258-z.pdf

    Article  PubMed  PubMed Central  Google Scholar 

  27. Barberio M, Longo F, Fiorillo C et al (2020) HYPerspectral enhanced reality (HYPER): a physiology-based surgical guidance tool. Surg Endosc 34(4):1736–1744

    Article  Google Scholar 

  28. Barberio M, Felli E, Seyller E et al (2020) Quantitative fluorescence angiography versus hyperspectral imaging to assess bowel ischemia: A comparative study in enhanced reality. Surgery. https://doi.org/10.1016/j.surg.2020.02.008

    Article  PubMed  Google Scholar 

  29. Schlagowski AI, Singh F, Charles AL et al (2014) Mitochondrial uncoupling reduces exercise capacity despite several skeletal muscle metabolic adaptations. J Appl Physiol 116(4):364–375

    Article  CAS  Google Scholar 

  30. Diana M, Noll E, Diemunsch P et al (2015) Metabolism-guided bowel resection: potential role and accuracy of instant capillary lactates to identify the optimal resection site. Surg Innov 22(5):453–461

    Article  Google Scholar 

  31. Hayami S, Matsuda K, Iwamoto H et al (2019) Visualization and quantification of anastomotic perfusion in colorectal surgery using near-infrared fluorescence. Tech Coloproctol 23(10):973–980

    Article  CAS  Google Scholar 

  32. Agnus V, Pesce A, Boni L et al (2019) Fluorescence-based cholangiography: preliminary results from the IHU-IRCAD-EAES EURO-FIGS registry. Surg Endosc. https://doi.org/10.1007/s00464-019-07157-3

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Sauria Nuth and Laura Roth, clinical research assistants, for their assistance with data collection and study management. Additionally, the authors would like to thank Guy Temporal and Christopher Burel, professionals in medical English proofreading, for their help in reviewing the manuscript. The authors would also like to thank the ADIRAL (Association d’Aide aux Insuffisants Respiratoires d’ALsace) for its kind contribution in the acquisition of the Oroboros instrument.

Funding

This study was funded by a Grant of the ARC Foundation (https://www.fondation-arc.org/), via the ELIOS Grant (PI: Michele Diana).

Author information

Authors and Affiliations

  1. Department of General, Digestive, and Endocrine Surgery, University Hospital of Strasbourg, 1, place de l’Hôpital, 67091, Strasbourg, France

    Antonio D’Urso, Didier Mutter & Michele Diana

  2. IHU-Strasbourg, Institute of Image-Guided Surgery, Strasbourg, France

    Vincent Agnus, Manuel Barberio, Barbara Seeliger, Francesco Marchegiani, Jacques Marescaux, Didier Mutter & Michele Diana

  3. Institute of Physiology, EA3072, Mitochondria and Oxidative Stress, University of Strasbourg, Strasbourg, France

    Anne-Laure Charles, Bernard Geny, Didier Mutter & Michele Diana

  4. IRCAD, Research Institute Against Digestive Cancer, Strasbourg, France

    Jacques Marescaux & Michele Diana

  5. ICube Laboratory, Photonics Instrumentation for Health, Strasbourg, France

    Michele Diana

Authors
  1. Antonio D’Urso
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vincent Agnus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manuel Barberio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Barbara Seeliger
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Francesco Marchegiani
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anne-Laure Charles
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bernard Geny
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jacques Marescaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Didier Mutter
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Michele Diana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michele Diana.

Ethics declarations

Disclosures

Michele Diana is member of the Advisory Board of Diagnostic Green and is the recipient of the ELIOS grant from the ARC Foundation. Jacques Marescaux is the President of the IRCAD Institute, which is partly funded by KARL STORZ and Medtronic. Antonio D’Urso, Vincent Agnus, Manuel Barberio, Barbara Seeliger, Francesco Marchegiani, Anne-Laure Charles, Bernard Geny, and Didier Mutter 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.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (MP4 157896 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

D’Urso, A., Agnus, V., Barberio, M. et al. Computer-assisted quantification and visualization of bowel perfusion using fluorescence-based enhanced reality in left-sided colonic resections. Surg Endosc 35, 4321–4331 (2021). https://doi.org/10.1007/s00464-020-07922-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00464-020-07922-9

Keywords

Search

Navigation