Skip to main content
Top
Published in: Surgical Endoscopy 6/2019

01-06-2019 | 2018 SAGES Oral

Discrimination between arterial and venous bowel ischemia by computer-assisted analysis of the fluorescent signal

Authors: Giuseppe Quero, Alfonso Lapergola, Manuel Barberio, Barbara Seeliger, Paola Saccomandi, Ludovica Guerriero, Didier Mutter, Alend Saadi, Marc Worreth, Jacques Marescaux, Vincent Agnus, Michele Diana

Published in: Surgical Endoscopy | Issue 6/2019

Login to get access

Abstract

Background

Arterial blood supply deficiency and venous congestion both play a role in anastomotic complications. Our aim was to evaluate a software-based analysis of the fluorescence signal to recognize the patterns of bowel ischemia.

Methods

In 18 pigs, two clips were applied on the inferior mesenteric artery (group A: n = 6) or vein (group V: n = 6) or on both (group A–V: n = 6). Three regions of interest (ROIs) were identified on the sigmoid: P = proximal to the first clip; C = central, between the two clips; and D = distal to the second clip. Indocyanine Green was injected intravenously. The fluorescence signal was captured by means of a near-infrared laparoscope. The time-to-peak (seconds) and the maximum fluorescence intensity were recorded using software. A normalized fluorescence intensity unit (NFIU: 0-to-1) was attributed, using a reference card. The NFIU’s over-time variations were computed every 10 min for 50 min. Capillary lactates were measured on the sigmoid at the 3 ROIs. Various machine learning algorithms were applied for ischemia patterns recognition.

Results

The time-to-peak at the ischemic ROI C was significantly longer in group A versus V (20.1 ± 13 vs. 8.43 ± 3.7; p = 0.04) and in group A–V versus V (20.71 ± 11.6 vs. 8.43 ± 3.7; p = 0.03). The maximal NIFU at ROI C, was higher in the V group (1.01 ± 0.21) when compared to A (0.61 ± 0.11; p = 0.002) and A–V (0.41 ± 0.2; p = 0.0005). Capillary lactates at ROI C were lower in V (1.3 ± 0.6) than in A (1.9 ± 0.5; p = 0.0071), and A–V (2.6 ± 1.5; p = 0.034). The K nearest neighbor and the Linear SVM algorithms provided both an accuracy of 75% in discriminating between A versus V and 85% in discriminating A versus A–V. The accuracy dropped to 70% when the ML had to identify the ROI and the type of ischemia simultaneously.

Conclusions

The computer-assisted dynamic analysis of the fluorescence signal enables the discrimination between different bowel ischemia models.
Literature
1.
go back to reference van Manen L, Handgraaf HJM, Diana M, Dijkstra J, Ishizawa T, Vahrmeijer AL, Mieog JSD (2018) A practical guide for the use of indocyanine green and methylene blue in fluorescence-guided abdominal surgery. J Surg Oncol 118:283–300CrossRefPubMedPubMedCentral van Manen L, Handgraaf HJM, Diana M, Dijkstra J, Ishizawa T, Vahrmeijer AL, Mieog JSD (2018) A practical guide for the use of indocyanine green and methylene blue in fluorescence-guided abdominal surgery. J Surg Oncol 118:283–300CrossRefPubMedPubMedCentral
2.
go back to reference Degett TH, Andersen HS, Gogenur I (2016) Indocyanine green fluorescence angiography for intraoperative assessment of gastrointestinal anastomotic perfusion: a systematic review of clinical trials. Langenbecks Arch Surg 401:767–775CrossRefPubMed Degett TH, Andersen HS, Gogenur I (2016) Indocyanine green fluorescence angiography for intraoperative assessment of gastrointestinal anastomotic perfusion: a systematic review of clinical trials. Langenbecks Arch Surg 401:767–775CrossRefPubMed
3.
go back to reference 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 22:15–23CrossRefPubMed 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 22:15–23CrossRefPubMed
4.
go back to reference Ohi M, Toiyama Y, Mohri Y, Saigusa S, Ichikawa T, Shimura T, Yasuda H, Okita Y, Yoshiyama S, Kobayashi M, Araki T, Inoue Y, Kusunoki M (2017) Prevalence of anastomotic leak and the impact of indocyanine green fluorescein imaging for evaluating blood flow in the gastric conduit following esophageal cancer surgery. Esophagus 14:351–359CrossRefPubMedPubMedCentral Ohi M, Toiyama Y, Mohri Y, Saigusa S, Ichikawa T, Shimura T, Yasuda H, Okita Y, Yoshiyama S, Kobayashi M, Araki T, Inoue Y, Kusunoki M (2017) Prevalence of anastomotic leak and the impact of indocyanine green fluorescein imaging for evaluating blood flow in the gastric conduit following esophageal cancer surgery. Esophagus 14:351–359CrossRefPubMedPubMedCentral
7.
go back to reference Diana M, Agnus V, Halvax P, Liu YY, Dallemagne B, Schlagowski AI, Geny B, Diemunsch P, Lindner V, Marescaux J (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:e169–e176CrossRefPubMed Diana M, Agnus V, Halvax P, Liu YY, Dallemagne B, Schlagowski AI, Geny B, Diemunsch P, Lindner V, Marescaux J (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:e169–e176CrossRefPubMed
8.
go back to reference Diana M, Dallemagne B, Chung H, Nagao Y, Halvax P, Agnus V, Soler L, Lindner V, Demartines N, Diemunsch P, Geny B, Swanstrom L, Marescaux J (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 28:3224–3233CrossRefPubMed Diana M, Dallemagne B, Chung H, Nagao Y, Halvax P, Agnus V, Soler L, Lindner V, Demartines N, Diemunsch P, Geny B, Swanstrom L, Marescaux J (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 28:3224–3233CrossRefPubMed
9.
go back to reference Diana M, Halvax P, Dallemagne B, Nagao Y, Diemunsch P, Charles AL, Agnus V, Soler L, Demartines N, Lindner V, Geny B, Marescaux J (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, Nagao Y, Diemunsch P, Charles AL, Agnus V, Soler L, Demartines N, Lindner V, Geny B, Marescaux J (2014) Real-time navigation by fluorescence-based enhanced reality for precise estimation of future anastomotic site in digestive surgery. Surg Endosc 28:3108–3118CrossRefPubMed
10.
go back to reference Diana M, Noll E, Agnus V, Liu YY, Kong SH, Legner A, Diemunsch P, Marescaux J (2017) Reply to letter: “enhanced reality fluorescence videography to assess bowel perfusion: the cybernetic eye”. Ann Surg 265:e49–e52CrossRefPubMed Diana M, Noll E, Agnus V, Liu YY, Kong SH, Legner A, Diemunsch P, Marescaux J (2017) Reply to letter: “enhanced reality fluorescence videography to assess bowel perfusion: the cybernetic eye”. Ann Surg 265:e49–e52CrossRefPubMed
11.
go back to reference Diana M, Noll E, Diemunsch P, Dallemagne B, Benahmed MA, Agnus V, Soler L, Barry B, Namer IJ, Demartines N, Charles AL, Geny B, Marescaux J (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259:700–707CrossRefPubMed Diana M, Noll E, Diemunsch P, Dallemagne B, Benahmed MA, Agnus V, Soler L, Barry B, Namer IJ, Demartines N, Charles AL, Geny B, Marescaux J (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259:700–707CrossRefPubMed
12.
go back to reference Lee KT, Mun GH (2017) Benefits of superdrainage using SIEV in DIEP flap breast reconstruction: a systematic review and meta-analysis. Microsurgery 37:75–83CrossRefPubMed Lee KT, Mun GH (2017) Benefits of superdrainage using SIEV in DIEP flap breast reconstruction: a systematic review and meta-analysis. Microsurgery 37:75–83CrossRefPubMed
13.
go back to reference Fujioka M, Hayashida K, Fukui K, Ishiyama S, Saijo H, Taniguchi K (2017) Venous superdrained gastric tube pull-up procedure for hypopharyngeal and cervical esophageal reconstruction reduces postoperative anastomotic leakage and stricture. Dis Esophagus 30:1–6CrossRefPubMed Fujioka M, Hayashida K, Fukui K, Ishiyama S, Saijo H, Taniguchi K (2017) Venous superdrained gastric tube pull-up procedure for hypopharyngeal and cervical esophageal reconstruction reduces postoperative anastomotic leakage and stricture. Dis Esophagus 30:1–6CrossRefPubMed
15.
go back to reference Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, Group NCRRGW (2010) Animal research: reporting in vivo experiments: the ARRIVE guidelines. J Gene Med 12:561–563CrossRefPubMed Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, Group NCRRGW (2010) Animal research: reporting in vivo experiments: the ARRIVE guidelines. J Gene Med 12:561–563CrossRefPubMed
16.
go back to reference Diana M, Halvax P, Pop R, Schlagowski I, Bour G, Liu YY, Legner A, Diemunsch P, Geny B, Dallemagne B, Beaujeux R, Demartines N, Marescaux J (2015) Gastric supply manipulation to modulate ghrelin production and enhance vascularization to the cardia: proof of the concept in a porcine model. Surg Innov 22:5–14CrossRefPubMed Diana M, Halvax P, Pop R, Schlagowski I, Bour G, Liu YY, Legner A, Diemunsch P, Geny B, Dallemagne B, Beaujeux R, Demartines N, Marescaux J (2015) Gastric supply manipulation to modulate ghrelin production and enhance vascularization to the cardia: proof of the concept in a porcine model. Surg Innov 22:5–14CrossRefPubMed
17.
go back to reference Diana M, Noll E, Legner A, Kong SH, Liu YY, Schiraldi L, Marchegiani F, Bano J, Geny B, Charles AL, Dallemagne B, Lindner V, Mutter D, Diemunsch P, Marescaux J (2018) Impact of valve-less vs. standard insufflation on pneumoperitoneum volume, inflammation, and peritoneal physiology in a laparoscopic sigmoid resection experimental model. Surg Endosc 32:3215–3224CrossRefPubMed Diana M, Noll E, Legner A, Kong SH, Liu YY, Schiraldi L, Marchegiani F, Bano J, Geny B, Charles AL, Dallemagne B, Lindner V, Mutter D, Diemunsch P, Marescaux J (2018) Impact of valve-less vs. standard insufflation on pneumoperitoneum volume, inflammation, and peritoneal physiology in a laparoscopic sigmoid resection experimental model. Surg Endosc 32:3215–3224CrossRefPubMed
18.
go back to reference Pedregosa F, Gaël V, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V, Vanderplas J, Passos A, Cournapeau D, Brucher M, Perrot M, Duchesnay É (2011) Scikit-learn: machine learning in python. J Mach Learn Res 12:2825–2830 Pedregosa F, Gaël V, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V, Vanderplas J, Passos A, Cournapeau D, Brucher M, Perrot M, Duchesnay É (2011) Scikit-learn: machine learning in python. J Mach Learn Res 12:2825–2830
19.
go back to reference Devijver PA, Kittler J (1982) Pattern recognition: a statistical approach. Prentice-Hall, London Devijver PA, Kittler J (1982) Pattern recognition: a statistical approach. Prentice-Hall, London
20.
go back to reference Ris F, Liot E, Buchs NC, Kraus R, Ismael G, Belfontali V, Douissard J, Cunningham C, Lindsey I, Guy R, Jones O, George B, Morel P, Mortensen NJ, Hompes R, Cahill RA, Near-Infrared Anastomotic Perfusion Assessment Network V (2018) Multicentre phase II trial of near-infrared imaging in elective colorectal surgery. Br J Surg 105:1359–1367CrossRefPubMedPubMedCentral Ris F, Liot E, Buchs NC, Kraus R, Ismael G, Belfontali V, Douissard J, Cunningham C, Lindsey I, Guy R, Jones O, George B, Morel P, Mortensen NJ, Hompes R, Cahill RA, Near-Infrared Anastomotic Perfusion Assessment Network V (2018) Multicentre phase II trial of near-infrared imaging in elective colorectal surgery. Br J Surg 105:1359–1367CrossRefPubMedPubMedCentral
23.
go back to reference Diana M (2018) Fluorescence-guided surgery applied to the digestive system: the cybernetic eye to see the invisible. Cir Esp 96:65–68CrossRefPubMed Diana M (2018) Fluorescence-guided surgery applied to the digestive system: the cybernetic eye to see the invisible. Cir Esp 96:65–68CrossRefPubMed
24.
go back to reference Koyanagi K, Ozawa S, Oguma J, Kazuno A, Yamazaki Y, Ninomiya Y, Ochiai H, Tachimori Y (2016) Blood flow speed of the gastric conduit assessed by indocyanine green fluorescence: new predictive evaluation of anastomotic leakage after esophagectomy. Medicine (Baltimore) 95:e4386CrossRef Koyanagi K, Ozawa S, Oguma J, Kazuno A, Yamazaki Y, Ninomiya Y, Ochiai H, Tachimori Y (2016) Blood flow speed of the gastric conduit assessed by indocyanine green fluorescence: new predictive evaluation of anastomotic leakage after esophagectomy. Medicine (Baltimore) 95:e4386CrossRef
25.
go back to reference Wada T, Kawada K, Takahashi R, Yoshitomi M, Hida K, Hasegawa S, Sakai Y (2017) ICG fluorescence imaging for quantitative evaluation of colonic perfusion in laparoscopic colorectal surgery. Surgical endoscopy 31:4184–4193CrossRefPubMed Wada T, Kawada K, Takahashi R, Yoshitomi M, Hida K, Hasegawa S, Sakai Y (2017) ICG fluorescence imaging for quantitative evaluation of colonic perfusion in laparoscopic colorectal surgery. Surgical endoscopy 31:4184–4193CrossRefPubMed
26.
go back to reference Selka F, Agnus V, Nicolau S, Bessaid A, Soler L, Marescaux J, Diana M (2014) Fluorescence-based enhanced reality for colorectal endoscopic surgery. Biomedical Image Registration, London, pp 114–123 Selka F, Agnus V, Nicolau S, Bessaid A, Soler L, Marescaux J, Diana M (2014) Fluorescence-based enhanced reality for colorectal endoscopic surgery. Biomedical Image Registration, London, pp 114–123
27.
go back to reference Diana M, Noll E, Diemunsch P, Moussallieh FM, Namer IJ, Charles AL, Lindner V, Agnus V, Geny B, Marescaux J (2015) Metabolism-guided bowel resection: potential role and accuracy of instant capillary lactates to identify the optimal resection site. Surg Innov 22:453–461CrossRefPubMed Diana M, Noll E, Diemunsch P, Moussallieh FM, Namer IJ, Charles AL, Lindner V, Agnus V, Geny B, Marescaux J (2015) Metabolism-guided bowel resection: potential role and accuracy of instant capillary lactates to identify the optimal resection site. Surg Innov 22:453–461CrossRefPubMed
28.
go back to reference Diana M, Pop R, Beaujeux R, Dallemagne B, Halvax P, Schlagowski I, Liu YY, Diemunsch P, Geny B, Lindner V, Marescaux J (2015) Embolization of arterial gastric supply in obesity (EMBARGO): an endovascular approach in the management of morbid obesity. proof of the concept in the porcine model. Obes Surg 25:550–558CrossRefPubMed Diana M, Pop R, Beaujeux R, Dallemagne B, Halvax P, Schlagowski I, Liu YY, Diemunsch P, Geny B, Lindner V, Marescaux J (2015) Embolization of arterial gastric supply in obesity (EMBARGO): an endovascular approach in the management of morbid obesity. proof of the concept in the porcine model. Obes Surg 25:550–558CrossRefPubMed
29.
go back to reference Cruz RJ Jr, Garrido AG, Ribeiro CM, Harada T, Rocha-e-Silva M (2010) Regional blood flow distribution and oxygen metabolism during mesenteric ischemia and congestion. J Surg Res 161:54–61CrossRefPubMed Cruz RJ Jr, Garrido AG, Ribeiro CM, Harada T, Rocha-e-Silva M (2010) Regional blood flow distribution and oxygen metabolism during mesenteric ischemia and congestion. J Surg Res 161:54–61CrossRefPubMed
30.
go back to reference Guzman-de la Garza FJ, Camara-Lemarroy CR, Alarcon-Galvan G, Cordero-Perez P, Munoz-Espinosa LE, Fernandez-Garza NE (2009) Different patterns of intestinal response to injury after arterial, venous or arteriovenous occlusion in rats. World J Gastroenterol 15:3901–3907CrossRefPubMedPubMedCentral Guzman-de la Garza FJ, Camara-Lemarroy CR, Alarcon-Galvan G, Cordero-Perez P, Munoz-Espinosa LE, Fernandez-Garza NE (2009) Different patterns of intestinal response to injury after arterial, venous or arteriovenous occlusion in rats. World J Gastroenterol 15:3901–3907CrossRefPubMedPubMedCentral
31.
go back to reference Yano K, Hata Y, Matsuka K, Ito O, Matsuda H (1994) Time limits for intestinal ischemia and congestion: an experimental study in rats. Ann Plast Surg 32:310–314CrossRefPubMed Yano K, Hata Y, Matsuka K, Ito O, Matsuda H (1994) Time limits for intestinal ischemia and congestion: an experimental study in rats. Ann Plast Surg 32:310–314CrossRefPubMed
32.
go back to reference Kimura M, Kataoka M, Kuwabara Y, Sato A, Sugiura M, Fujii Y (2003) Real-time energy metabolism of intestine during arterial versus venous occlusion in the rat. J Gastroenterol 38:849–853CrossRefPubMed Kimura M, Kataoka M, Kuwabara Y, Sato A, Sugiura M, Fujii Y (2003) Real-time energy metabolism of intestine during arterial versus venous occlusion in the rat. J Gastroenterol 38:849–853CrossRefPubMed
33.
go back to reference Vincenti M, Behrends M, Dang K, Park YH, Hirose R, Blasi-Ibanez A, Liu T, Serkova NJ, Niemann CU (2010) Induction of intestinal ischemia reperfusion injury by portal vein outflow occlusion in rats. J Gastroenterol 45:1103–1110CrossRefPubMed Vincenti M, Behrends M, Dang K, Park YH, Hirose R, Blasi-Ibanez A, Liu T, Serkova NJ, Niemann CU (2010) Induction of intestinal ischemia reperfusion injury by portal vein outflow occlusion in rats. J Gastroenterol 45:1103–1110CrossRefPubMed
34.
go back to reference Nasser A, Fourman MS, Gersch RP, Phillips BT, Hsi HK, Khan SU, Gelfand MA, Dagum AB, Bui DT (2015) Utilizing indocyanine green dye angiography to detect simulated flap venous congestion in a novel experimental rat model. J Reconstr Microsurg 31:590–596CrossRefPubMed Nasser A, Fourman MS, Gersch RP, Phillips BT, Hsi HK, Khan SU, Gelfand MA, Dagum AB, Bui DT (2015) Utilizing indocyanine green dye angiography to detect simulated flap venous congestion in a novel experimental rat model. J Reconstr Microsurg 31:590–596CrossRefPubMed
35.
go back to reference Bodin F, Diana M, Koutsomanis A, Robert E, Marescaux J, Bruant-Rodier C (2015) Porcine model for free-flap breast reconstruction training. J Plast Reconstr Aesthet Surg 68:1402–1409CrossRefPubMed Bodin F, Diana M, Koutsomanis A, Robert E, Marescaux J, Bruant-Rodier C (2015) Porcine model for free-flap breast reconstruction training. J Plast Reconstr Aesthet Surg 68:1402–1409CrossRefPubMed
36.
go back to reference Milstein DM, Ince C, Gisbertz SS, Boateng KB, Geerts BF, Hollmann MW, van Berge Henegouwen MI, Veelo DP (2016) Laser speckle contrast imaging identifies ischemic areas on gastric tube reconstructions following esophagectomy. Medicine (Baltimore) 95:e3875CrossRef Milstein DM, Ince C, Gisbertz SS, Boateng KB, Geerts BF, Hollmann MW, van Berge Henegouwen MI, Veelo DP (2016) Laser speckle contrast imaging identifies ischemic areas on gastric tube reconstructions following esophagectomy. Medicine (Baltimore) 95:e3875CrossRef
37.
go back to reference Diana M, Hubner M, Vuilleumier H, Bize P, Denys A, Demartines N, Schafer M (2011) Redistribution of gastric blood flow by embolization of gastric arteries before esophagectomy. Ann Thorac Surg 91:1546–1551CrossRefPubMed Diana M, Hubner M, Vuilleumier H, Bize P, Denys A, Demartines N, Schafer M (2011) Redistribution of gastric blood flow by embolization of gastric arteries before esophagectomy. Ann Thorac Surg 91:1546–1551CrossRefPubMed
38.
go back to reference Yoshimi F, Asato Y, Ikeda S, Okamoto K, Komuro Y, Imura J, Itabashi M (2006) Using the supercharge technique to additionally revascularize the gastric tube after a subtotal esophagectomy for esophageal cancer. Am J Surg 191:284–287CrossRefPubMed Yoshimi F, Asato Y, Ikeda S, Okamoto K, Komuro Y, Imura J, Itabashi M (2006) Using the supercharge technique to additionally revascularize the gastric tube after a subtotal esophagectomy for esophageal cancer. Am J Surg 191:284–287CrossRefPubMed
39.
go back to reference Kono K, Sugai H, Omata H, Fujii H (2007) Transient bloodletting of the short gastric vein in the reconstructed gastric tube improves gastric microcirculation during esophagectomy. World J Surg 31:780–784 (discussion 785–786)CrossRefPubMed Kono K, Sugai H, Omata H, Fujii H (2007) Transient bloodletting of the short gastric vein in the reconstructed gastric tube improves gastric microcirculation during esophagectomy. World J Surg 31:780–784 (discussion 785–786)CrossRefPubMed
Metadata
Title
Discrimination between arterial and venous bowel ischemia by computer-assisted analysis of the fluorescent signal
Authors
Giuseppe Quero
Alfonso Lapergola
Manuel Barberio
Barbara Seeliger
Paola Saccomandi
Ludovica Guerriero
Didier Mutter
Alend Saadi
Marc Worreth
Jacques Marescaux
Vincent Agnus
Michele Diana
Publication date
01-06-2019
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 6/2019
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-018-6512-6

Other articles of this Issue 6/2019

Surgical Endoscopy 6/2019 Go to the issue