Skip to main content
Top
Published in: Langenbeck's Archives of Surgery 4/2017

01-06-2017 | ORIGINAL ARTICLE

Quantification of fluorescence angiography in a porcine model

Authors: Nikolaj Nerup, Helene Schou Andersen, Rikard Ambrus, Rune Broni Strandby, Morten Bo Søndergaard Svendsen, Mads Holst Madsen, Lars Bo Svendsen, Michael Patrick Achiam

Published in: Langenbeck's Archives of Surgery | Issue 4/2017

Login to get access

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.
Appendix
Available only for authorised users
Literature
2.
go back to reference 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 139PubMed 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 139PubMed
4.
go back to reference Boni L, David G, Mangano A et al (2015) Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc 29:2046–2055CrossRefPubMed Boni L, David G, Mangano A et al (2015) Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc 29:2046–2055CrossRefPubMed
5.
go back to reference 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 28:3108–3118CrossRefPubMed 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 28:3108–3118CrossRefPubMed
6.
go back to reference 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 21:332–338CrossRef 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 21:332–338CrossRef
7.
go back to reference 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 1030-1021CrossRefPubMedPubMedCentral 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 1030-1021CrossRefPubMedPubMedCentral
8.
go back to reference 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 19:486–493CrossRefPubMed 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 19:486–493CrossRefPubMed
9.
go back to reference Ishizawa T, Bandai Y, Ijichi M et al (2010) Fluorescent cholangiography illuminating the biliary tree during laparoscopic cholecystectomy. Br J Surg 97:1369–1377CrossRefPubMed Ishizawa T, Bandai Y, Ijichi M et al (2010) Fluorescent cholangiography illuminating the biliary tree during laparoscopic cholecystectomy. Br J Surg 97:1369–1377CrossRefPubMed
10.
go back to reference 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. 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.
go back to reference Thompson SK, Chang EY, Jobe BA (2006) Clinical review: healing in gastrointestinal anastomoses, part I. Microsurgery 26:131–136CrossRefPubMed Thompson SK, Chang EY, Jobe BA (2006) Clinical review: healing in gastrointestinal anastomoses, part I. Microsurgery 26:131–136CrossRefPubMed
12.
go back to reference Chadi SA, Fingerhut A, Berho M, et al. (2016) Emerging trends in the etiology, prevention, and treatment of gastrointestinal anastomotic leakage. J Gastrointest Surg. 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.
go back to reference 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 262:972–980CrossRefPubMed 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 262:972–980CrossRefPubMed
14.
go back to reference 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 253:890–899CrossRefPubMed 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 253:890–899CrossRefPubMed
15.
go back to reference Karliczek A, Harlaar NJ, Zeebregts CJ et al (2009) Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Color Dis 24:569–576CrossRef Karliczek A, Harlaar NJ, Zeebregts CJ et al (2009) Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Color Dis 24:569–576CrossRef
16.
go back to reference 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 3:59–69CrossRefPubMedPubMedCentral 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 3:59–69CrossRefPubMedPubMedCentral
17.
go back to reference Heymann MA, Payne BD, Hoffman JI, Rudolph AM (1977) Blood flow measurements with radionuclide-labeled particles. Prog Cardiovasc Dis 20:55–79CrossRefPubMed Heymann MA, Payne BD, Hoffman JI, Rudolph AM (1977) Blood flow measurements with radionuclide-labeled particles. Prog Cardiovasc Dis 20:55–79CrossRefPubMed
18.
go back to reference 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 47:203–209CrossRefPubMed 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 47:203–209CrossRefPubMed
19.
go back to reference 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–H116PubMed 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–H116PubMed
20.
go back to reference 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 35:49–57CrossRefPubMed 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 35:49–57CrossRefPubMed
21.
go back to reference Diana M, Noll E, Diemunsch P et al (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259:700–707CrossRefPubMed Diana M, Noll E, Diemunsch P et al (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259:700–707CrossRefPubMed
22.
go back to reference 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 37:1549–1551CrossRefPubMed 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 37:1549–1551CrossRefPubMed
23.
go back to reference Altman DG, Bland JM (1983) Measurement in medicine: the analysis of method comparison studies. The Statistician 32:307CrossRef Altman DG, Bland JM (1983) Measurement in medicine: the analysis of method comparison studies. The Statistician 32:307CrossRef
24.
go back to reference 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):16–21CrossRef 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):16–21CrossRef
25.
go back to reference 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 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
26.
go back to reference 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 365:1718–1726CrossRefPubMed 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 365:1718–1726CrossRefPubMed
27.
go back to reference 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–e667CrossRef 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–e667CrossRef
28.
go back to reference 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 81:580–584PubMed 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 81:580–584PubMed
29.
go back to reference 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 395:1025–1030CrossRef 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 395:1025–1030CrossRef
Metadata
Title
Quantification of fluorescence angiography in a porcine model
Authors
Nikolaj Nerup
Helene Schou Andersen
Rikard Ambrus
Rune Broni Strandby
Morten Bo Søndergaard Svendsen
Mads Holst Madsen
Lars Bo Svendsen
Michael Patrick Achiam
Publication date
01-06-2017
Publisher
Springer Berlin Heidelberg
Published in
Langenbeck's Archives of Surgery / Issue 4/2017
Print ISSN: 1435-2443
Electronic ISSN: 1435-2451
DOI
https://doi.org/10.1007/s00423-016-1531-z

Other articles of this Issue 4/2017

Langenbeck's Archives of Surgery 4/2017 Go to the issue