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Quantification of fluorescence angiography in a porcine model

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Abstract

Purpose

There is no consensus on how to quantify indocyanine green (ICG) fluorescence angiography. The aim of the present study was to establish and gather validity evidence for a method of quantifying fluorescence angiography, to assess organ perfusion.

Methods

Laparotomy was performed on seven pigs, with two regions of interest (ROIs) marked. ICG and neutron-activated microspheres were administered and the stomach was illuminated in the near-infrared range, parallel to continuous recording of fluorescence signal. Tissue samples from the ROIs were sent for quantification of microspheres to calculate the regional blood flow. A software system was developed to assess the fluorescent recordings quantitatively, and each quantitative parameter was compared with the regional blood flow. The parameter with the strongest correlation was then compared with results from an independently developed algorithm, to evaluate reproducibility.

Results

A strong correlation was found between regional blood flow and the slope of the fluorescence curves (ROI I: Pearson r = 0.97, p < 0.001; ROI II: 0.96, p < 0.001) as the normalized slope (ROI I: Pearson r = 0.92, p = 0.004; ROI II: r = 0.96, p = 0.001). There was acceptable correlation of the slope of the curve between two independently developed algorithms (ROI I+II: Pearson r = 0.83, p < 0.001), and good resemblance was found with the Bland-Altman method, with no proportional bias.

Conclusions

Perfusion assessment with quantitative indocyanine green fluorescence angiography is not only feasible but easy to perform with commercially available equipment and readily accessible software.

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References

  1. Owens SL (1996) Indocyanine green angiography. Br J Ophthalmol 80:263–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V (2003) Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery 52:132–139 discussion 139

    PubMed  Google Scholar 

  3. Alander JT, Kaartinen I, Laakso A et al (2012) A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012:940585

    Article  PubMed  PubMed Central  Google Scholar 

  4. Boni L, David G, Mangano A et al (2015) Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc 29:2046–2055

    Article  PubMed  Google Scholar 

  5. 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 28:3108–3118

    Article  PubMed  Google Scholar 

  6. Toens C, Krones CJ, Blum U et al (2006) Validation of IC-VIEW fluorescence videography in a rabbit model of mesenteric ischaemia and reperfusion. Int J Color Dis 21:332–338

    Article  CAS  Google Scholar 

  7. Towle EL, Richards LM, Kazmi SM, Fox DJ, Dunn AK (2012) Comparison of indocyanine green angiography and laser speckle contrast imaging for the assessment of vasculature perfusion. Neurosurgery 71:1023–1030 discussion 1030-1021

    Article  PubMed  PubMed Central  Google Scholar 

  8. Yuasa Y, Seike J, Yoshida T et al (2012) Sentinel lymph node biopsy using intraoperative indocyanine green fluorescence imaging navigated with preoperative CT lymphography for superficial esophageal cancer. Ann Surg Oncol 19:486–493

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  10. Degett TH, Andersen HS, and Gogenur I (2016) Indocyanine green fluorescence angiography for intraoperative assessment of gastrointestinal anastomotic perfusion: a systematic review of clinical trials. Langenbecks Arch Surg.

  11. Thompson SK, Chang EY, Jobe BA (2006) Clinical review: healing in gastrointestinal anastomoses, part I. Microsurgery 26:131–136

    Article  PubMed  Google Scholar 

  12. Chadi SA, Fingerhut A, Berho M, et al. (2016) Emerging trends in the etiology, prevention, and treatment of gastrointestinal anastomotic leakage. J Gastrointest Surg.

  13. Markar S, Gronnier C, Duhamel A et al (2015) The impact of severe anastomotic leak on long-term survival and cancer recurrence after surgical resection for esophageal malignancy. Ann Surg 262:972–980

    Article  PubMed  Google Scholar 

  14. Mirnezami A, Mirnezami R, Chandrakumaran K et al (2011) Increased local recurrence and reduced survival from colorectal cancer following anastomotic leak: systematic review and meta-analysis. Ann Surg 253:890–899

    Article  PubMed  Google Scholar 

  15. Karliczek A, Harlaar NJ, Zeebregts CJ et al (2009) Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Color Dis 24:569–576

    Article  CAS  Google Scholar 

  16. Urbanavicius L, Pattyn P, de Putte DV, Venskutonis D (2011) How to assess intestinal viability during surgery: a review of techniques. World J Gastrointest Surg 3:59–69

    Article  PubMed  PubMed Central  Google Scholar 

  17. Heymann MA, Payne BD, Hoffman JI, Rudolph AM (1977) Blood flow measurements with radionuclide-labeled particles. Prog Cardiovasc Dis 20:55–79

    Article  CAS  PubMed  Google Scholar 

  18. Lange M, Hamahata A, Traber DL et al (2013) Multiple versus single injections of fluorescent microspheres for the determination of regional organ blood flow in septic sheep. Lab Anim 47:203–209

    Article  PubMed  Google Scholar 

  19. Reinhardt CP, Dalhberg S, Tries MA, Marcel R, Leppo JA (2001) Stable labeled microspheres to measure perfusion: validation of a neutron activation assay technique. Am J Physiol Heart Circ Physiol 280:H108–H116

    CAS  PubMed  Google Scholar 

  20. Levesque E, Martin E, Dudau D et al (2016) Current use and perspective of indocyanine green clearance in liver diseases. Anaesth Crit Care Pain Med 35:49–57

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  22. Woitzik J, Pena-Tapia PG, Schneider UC, Vajkoczy P, Thome C (2006) Cortical perfusion measurement by indocyanine-green videoangiography in patients undergoing hemicraniectomy for malignant stroke. Stroke 37:1549–1551

    Article  PubMed  Google Scholar 

  23. Altman DG, Bland JM (1983) Measurement in medicine: the analysis of method comparison studies. The Statistician 32:307

    Article  Google Scholar 

  24. James DR, Ris F, Yeung TM et al (2015) Fluorescence angiography in laparoscopic low rectal and anorectal anastomoses with pinpoint perfusion imaging—a critical appraisal with specific focus on leak risk reduction. Color Dis 17(Suppl 3):16–21

    Article  Google Scholar 

  25. 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(82–92):e81

    Google Scholar 

  26. Guillou PJ, Quirke P, Thorpe H et al (2005) Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet 365:1718–1726

    Article  PubMed  Google Scholar 

  27. Krarup PM, Jorgensen LN, Andreasen AH, Harling H, Danish Colorectal Cancer G (2012) A nationwide study on anastomotic leakage after colonic cancer surgery. Color Dis 14:e661–e667

    Article  Google Scholar 

  28. Protyniak B, Dinallo AM, Boyan WP Jr, Dressner RM, Arvanitis ML (2015) Intraoperative indocyanine green fluorescence angiography—an objective evaluation of anastomotic perfusion in colorectal surgery. Am Surg 81:580–584

    PubMed  Google Scholar 

  29. Kudszus S, Roesel C, Schachtrupp A, Hoer JJ (2010) Intraoperative laser fluorescence angiography in colorectal surgery: a noninvasive analysis to reduce the rate of anastomotic leakage. Langenbeck’s Arch Surg 395:1025–1030

    Article  Google Scholar 

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Acknowledgements

Equipment was kindly provided during the experiments by Karl Storz (Karl Storz GmbH and Co. KG, Tüttlingen, Germany). The study was supported by the Danish Cancer Research Foundation. The study sponsors had no role in the design of the study; the collection, analysis, or interpretation of the data; the writing of the manuscript; or the decision to submit the manuscript for publication.

Author contributions

Study conception and design: NN, HSA, RA, RBS, MBSS, MHM, LBS, and MA. Acquisition of data: NN, HSA, RA, RBS, MBSS, and MHM. Analysis and interpretation of data: NN, HSA, RA, RBS, MBSS, MHM, LBS, and MA. Drafting of manuscript: NN. Critical revision of manuscript: NN, HSA, RA, RBS, MBSS, MHM, LBS, and MA

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Authors and Affiliations

  1. Department of Surgical Gastroenterology, Copenhagen University Hospital Rigshospitalet, Blegdamsvej 9, 2100, Copenhagen Ø, Denmark

    Nikolaj Nerup, Rikard Ambrus, Rune Broni Strandby, Lars Bo Svendsen & Michael Patrick Achiam

  2. Center for Surgical Science (CSS), Zealand University Hospital, Lykkebækvej 1, 4600, Køge, Denmark

    Helene Schou Andersen

  3. Marine Biological Section, University of Copenhagen, Strandpromenaden 5, 3000, Elsinore, Denmark

    Morten Bo Søndergaard Svendsen

  4. Niels Bohr Institute, University of Copenhagen, Blegdamsvej 17, 2100, Copenhagen Ø, Denmark

    Mads Holst Madsen

Authors
  1. Nikolaj Nerup
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  2. Helene Schou Andersen
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  7. Lars Bo Svendsen
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  8. Michael Patrick Achiam
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Corresponding author

Correspondence to Nikolaj Nerup.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in animals were in accordance with the ethical standards of the institution, at which the studies were conducted. The study was conducted under the supervision of research veterinarians at the Department of Experimental Medicine, Panum Institute, University of Copenhagen and was approved by the Danish Animal Experiments Inspectorate (No. 2012-15-2934-00186).

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Nerup, N., Andersen, H.S., Ambrus, R. et al. Quantification of fluorescence angiography in a porcine model. Langenbecks Arch Surg 402, 655–662 (2017). https://doi.org/10.1007/s00423-016-1531-z

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  • DOI: https://doi.org/10.1007/s00423-016-1531-z

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