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Published in: Surgical Endoscopy 10/2021

Open Access 01-10-2021 | Esophagus Resection | 2020 EAES Oral

Quantitative serosal and mucosal optical imaging perfusion assessment in gastric conduits for esophageal surgery: an experimental study in enhanced reality

Authors: Manuel Barberio, Eric Felli, Margherita Pizzicannella, Vincent Agnus, Mahdi Al-Taher, Emilie Seyller, Yusef Moulla, Boris Jansen-Winkeln, Ines Gockel, Jacques Marescaux, Michele Diana

Published in: Surgical Endoscopy | Issue 10/2021

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Abstract

Introduction/objective

Gastric conduit (GC) is used for reconstruction after esophagectomy. Anastomotic leakage (AL) incidence remains high, given the extensive disruption of the gastric circulation. Currently, there is no reliable method to intraoperatively quantify gastric perfusion. Hyperspectral imaging (HSI) has shown its potential to quantify serosal StO2. Confocal laser endomicroscopy (CLE) allows for automatic mucosal microcirculation quantification as functional capillary density area (FCD-A). The aim of this study was to quantify serosal and mucosal GC’s microperfusion using HSI and CLE. Local capillary lactate (LCL) served as biomarker.

Methods

GC was formed in 5 pigs and serosal StO2% was quantified at 3 regions of interest (ROI) using HSI: fundus (ROI-F), greater curvature (ROI-C), and pylorus (ROI-P). After intravenous injection of sodium-fluorescein (0.5 g), CLE-based mucosal microperfusion was assessed at the corresponding ROIs, and LCLs were quantified via a lactate analyzer.

Results

StO2 and FCD-A at ROI-F (41 ± 10.6%, 3.3 ± 3.8, respectively) were significantly lower than ROI-C (68.2 ± 6.7%, p value: 0.005; 18.4 ± 7, p value: 0.01, respectively) and ROI-P (72 ± 10.4%, p value: 0.005; 15.7 ± 3.2 p value: 0.001). LCL value at ROI-F (9.6 ± 4.7 mmol/L) was significantly higher than at ROI-C (2.6 ± 1.2 mmol/L, p value: 0.04) and ROI-P (2.6 ± 1.3 mmol/L, p value: 0.04). No statistically significant difference was found in all metrics between ROI-C and ROI-P. StO2 correlated with FCD-A (Pearson’s r = 0.67). The LCL correlated negatively with both FCD-A (Spearman’s r =  − 0.74) and StO2 (Spearman’s r =  −  0.54).

Conclusions

GC formation causes a drop in serosal and mucosal fundic perfusion. HSI and CLE correlate well and might become useful intraoperative tools.
Literature
1.
go back to reference Low DE, Kuppusamy MK, Alderson D, Cecconello I, Chang AC, Darling G, Davies A, D’Journo XB, Gisbertz SS, Griffin SM (2019) Benchmarking complications associated with esophagectomy. Ann Surg 269:291–298CrossRef Low DE, Kuppusamy MK, Alderson D, Cecconello I, Chang AC, Darling G, Davies A, D’Journo XB, Gisbertz SS, Griffin SM (2019) Benchmarking complications associated with esophagectomy. Ann Surg 269:291–298CrossRef
2.
go back to reference Booka E, Takeuchi H, Suda K, Fukuda K, Nakamura R, Wada N, Kawakubo H, Kitagawa Y (2018) Meta-analysis of the impact of postoperative complications on survival after oesophagectomy for cancer. BJS Open 2:276–284CrossRef Booka E, Takeuchi H, Suda K, Fukuda K, Nakamura R, Wada N, Kawakubo H, Kitagawa Y (2018) Meta-analysis of the impact of postoperative complications on survival after oesophagectomy for cancer. BJS Open 2:276–284CrossRef
3.
go back to reference Morse BC, Simpson JP, Jones YR, Johnson BL, Knott BM, Kotrady JA (2013) Determination of independent predictive factors for anastomotic leak: analysis of 682 intestinal anastomoses. Am J Surg 206:950–956CrossRef Morse BC, Simpson JP, Jones YR, Johnson BL, Knott BM, Kotrady JA (2013) Determination of independent predictive factors for anastomotic leak: analysis of 682 intestinal anastomoses. Am J Surg 206:950–956CrossRef
4.
go back to reference Karliczek A, Harlaar N, Zeebregts C, Wiggers T, Baas P, Van Dam G (2009) Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Colorectal Dis 24:569–576CrossRef Karliczek A, Harlaar N, Zeebregts C, Wiggers T, Baas P, Van Dam G (2009) Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Colorectal Dis 24:569–576CrossRef
5.
go back to reference Urbanavičius L, Pattyn P, Van de Putte D, Venskutonis D (2011) How to assess intestinal viability during surgery: a review of techniques. World J Gastrointest Surg 3:59CrossRef Urbanavičius L, Pattyn P, Van de Putte D, Venskutonis D (2011) How to assess intestinal viability during surgery: a review of techniques. World J Gastrointest Surg 3:59CrossRef
6.
go back to reference Zehetner J, DeMeester SR, Alicuben ET, Oh DS, Lipham JC, Hagen JA, DeMeester TR (2015) Intraoperative assessment of perfusion of the gastric graft and correlation with anastomotic leaks after esophagectomy. Ann Surg 262:74CrossRef Zehetner J, DeMeester SR, Alicuben ET, Oh DS, Lipham JC, Hagen JA, DeMeester TR (2015) Intraoperative assessment of perfusion of the gastric graft and correlation with anastomotic leaks after esophagectomy. Ann Surg 262:74CrossRef
7.
go back to reference Noma K, Shirakawa Y, Kanaya N, Okada T, Maeda N, Ninomiya T, Tanabe S, Sakurama K, Fujiwara T (2018) Visualized evaluation of blood flow to the gastric conduit and complications in esophageal reconstruction. J Am Coll Surg 226:241–251CrossRef Noma K, Shirakawa Y, Kanaya N, Okada T, Maeda N, Ninomiya T, Tanabe S, Sakurama K, Fujiwara T (2018) Visualized evaluation of blood flow to the gastric conduit and complications in esophageal reconstruction. J Am Coll Surg 226:241–251CrossRef
8.
go back to reference Van Daele E, Van Nieuwenhove Y, Ceelen W, Vanhove C, Braeckman BP, Hoorens A, Van Limmen J, Varin O, Van de Putte D, Willaert W (2019) Near-infrared fluorescence guided esophageal reconstructive surgery: a systematic review. World J Gastrointest Oncol 11:250CrossRef Van Daele E, Van Nieuwenhove Y, Ceelen W, Vanhove C, Braeckman BP, Hoorens A, Van Limmen J, Varin O, Van de Putte D, Willaert W (2019) Near-infrared fluorescence guided esophageal reconstructive surgery: a systematic review. World J Gastrointest Oncol 11:250CrossRef
9.
go back to reference Jansen-Winkeln B, Holfert N, Köhler H, Moulla Y, Takoh J, Rabe S, Mehdorn M, Barberio M, Chalopin C, Neumuth T (2019) Determination of the transection margin during colorectal resection with hyperspectral imaging (HSI). Int J Colorectal Dis 34:731–739CrossRef Jansen-Winkeln B, Holfert N, Köhler H, Moulla Y, Takoh J, Rabe S, Mehdorn M, Barberio M, Chalopin C, Neumuth T (2019) Determination of the transection margin during colorectal resection with hyperspectral imaging (HSI). Int J Colorectal Dis 34:731–739CrossRef
10.
go back to reference Jansen-Winkeln B, Maktabi M, Takoh J, Rabe S, Barberio M, Köhler H, Neumuth T, Melzer A, Chalopin C, Gockel I (2018) Hyperspektral-imaging bei gastrointestinalen anastomosen. Der Chirurg 89:717–725CrossRef Jansen-Winkeln B, Maktabi M, Takoh J, Rabe S, Barberio M, Köhler H, Neumuth T, Melzer A, Chalopin C, Gockel I (2018) Hyperspektral-imaging bei gastrointestinalen anastomosen. Der Chirurg 89:717–725CrossRef
11.
go back to reference Köhler H, Jansen-Winkeln B, Maktabi M, Barberio M, Takoh J, Holfert N, Moulla Y, Niebisch S, Diana M, Neumuth T (2019) Evaluation of hyperspectral imaging (HSI) for the measurement of ischemic conditioning effects of the gastric conduit during esophagectomy. Surg Endosc 33:3775–3782CrossRef Köhler H, Jansen-Winkeln B, Maktabi M, Barberio M, Takoh J, Holfert N, Moulla Y, Niebisch S, Diana M, Neumuth T (2019) Evaluation of hyperspectral imaging (HSI) for the measurement of ischemic conditioning effects of the gastric conduit during esophagectomy. Surg Endosc 33:3775–3782CrossRef
12.
go back to reference Barberio M, Longo F, Fiorillo C, Seeliger B, Mascagni P, Agnus V, Lindner V, Geny B, Charles A-L, Gockel I (2019) HYPerspectral enhanced reality (HYPER): a physiology-based surgical guidance tool. Surg Endosc 34:1–9 Barberio M, Longo F, Fiorillo C, Seeliger B, Mascagni P, Agnus V, Lindner V, Geny B, Charles A-L, Gockel I (2019) HYPerspectral enhanced reality (HYPER): a physiology-based surgical guidance tool. Surg Endosc 34:1–9
15.
go back to reference Laemmel E, Genet M, Le Goualher G, Perchant A, Le Gargasson J-F, Vicaut E (2004) Fibered confocal fluorescence microscopy (Cell-viZio™) facilitates extended imaging in the field of microcirculation. J Vasc Res 41:400–411CrossRef Laemmel E, Genet M, Le Goualher G, Perchant A, Le Gargasson J-F, Vicaut E (2004) Fibered confocal fluorescence microscopy (Cell-viZio™) facilitates extended imaging in the field of microcirculation. J Vasc Res 41:400–411CrossRef
16.
go back to reference Diana M, Dallemagne B, Chung H, Nagao Y, Halvax P, Agnus V, Soler L, Lindner V, Demartines N, Diemunsch P (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 28:3224–3233CrossRef Diana M, Dallemagne B, Chung H, Nagao Y, Halvax P, Agnus V, Soler L, Lindner V, Demartines N, Diemunsch P (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 28:3224–3233CrossRef
17.
go back to reference Diana M, Noll E, Charles A-L, Diemunsch P, Geny B, Liu Y-Y, Marchegiani F, Schiraldi L, Agnus V, Lindner V (2017) Precision real-time evaluation of bowel perfusion: accuracy of confocal endomicroscopy assessment of stoma in a controlled hemorrhagic shock model. Surg Endosc 31:680–691CrossRef Diana M, Noll E, Charles A-L, Diemunsch P, Geny B, Liu Y-Y, Marchegiani F, Schiraldi L, Agnus V, Lindner V (2017) Precision real-time evaluation of bowel perfusion: accuracy of confocal endomicroscopy assessment of stoma in a controlled hemorrhagic shock model. Surg Endosc 31:680–691CrossRef
18.
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 12:561–563CrossRef 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 12:561–563CrossRef
19.
go back to reference Barberio M, Felli E, Seyller E, Longo F, Chand M, Gockel I, Geny B, Swanström L, Marescaux J, Agnus V (2020) Quantitative fluorescence angiography versus hyperspectral imaging to assess bowel ischemia: a comparative study in enhanced reality. Surgery 168:178CrossRef Barberio M, Felli E, Seyller E, Longo F, Chand M, Gockel I, Geny B, Swanström L, Marescaux J, Agnus V (2020) Quantitative fluorescence angiography versus hyperspectral imaging to assess bowel ischemia: a comparative study in enhanced reality. Surgery 168:178CrossRef
20.
go back to reference Diana M, Noll E, Diemunsch P, Moussallieh F-M, Namer I-J, Charles A-L, 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 22:453–461CrossRef Diana M, Noll E, Diemunsch P, Moussallieh F-M, Namer I-J, Charles A-L, 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 22:453–461CrossRef
21.
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–e176CrossRef 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–e176CrossRef
22.
go back to reference Diana M, Noll E, Diemunsch P, Dallemagne B, Benahmed MA, Agnus V, Soler L, Barry B, Namer IJ, Demartines N (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259:700–707CrossRef Diana M, Noll E, Diemunsch P, Dallemagne B, Benahmed MA, Agnus V, Soler L, Barry B, Namer IJ, Demartines N (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259:700–707CrossRef
23.
go back to reference Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V (2011) Scikit-learn: Machine learning in Python. J. Mach. Learn. Res. 12:2825–2830 Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V (2011) Scikit-learn: Machine learning in Python. J. Mach. Learn. Res. 12:2825–2830
24.
go back to reference Schröder W, Beckurts K, Stähler D, Stützer H, Fischer J, Hölscher A (2002) Microcirculatory changes associated with gastric tube formation in the pig. Eur Surg Res 34:411–417CrossRef Schröder W, Beckurts K, Stähler D, Stützer H, Fischer J, Hölscher A (2002) Microcirculatory changes associated with gastric tube formation in the pig. Eur Surg Res 34:411–417CrossRef
25.
go back to reference Irino T, Persson S, Lundell L, Nilsson M, Tsai JA, Rouvelas I (2018) Pulse oximetric assessment of anatomical vascular contribution to tissue perfusion in the gastric conduit. ANZ J Surg 88:727–732CrossRef Irino T, Persson S, Lundell L, Nilsson M, Tsai JA, Rouvelas I (2018) Pulse oximetric assessment of anatomical vascular contribution to tissue perfusion in the gastric conduit. ANZ J Surg 88:727–732CrossRef
26.
go back to reference Bludau M, Hölscher AH, Vallböhmer D, Gutschow C, Schröder W (2010) Ischemic conditioning of the gastric conduit prior to esophagectomy improves mucosal oxygen saturation. Ann Thorac Surg 90:1121–1126CrossRef Bludau M, Hölscher AH, Vallböhmer D, Gutschow C, Schröder W (2010) Ischemic conditioning of the gastric conduit prior to esophagectomy improves mucosal oxygen saturation. Ann Thorac Surg 90:1121–1126CrossRef
27.
go back to reference Bludau M, Vallböhmer D, Gutschow C, Hölscher A, Schröder W (2008) Quantitative measurement of gastric mucosal microcirculation using a combined laser Doppler flowmeter and spectrophotometer. Dis Esophagus 21:668–672CrossRef Bludau M, Vallböhmer D, Gutschow C, Hölscher A, Schröder W (2008) Quantitative measurement of gastric mucosal microcirculation using a combined laser Doppler flowmeter and spectrophotometer. Dis Esophagus 21:668–672CrossRef
28.
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 95:e387CrossRef 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 95:e387CrossRef
29.
go back to reference Nishikawa K, Fujita T, Yuda M, Tanaka Y, Matsumoto A, Tanishima Y, Hanyu N, Yanaga K (2018) Quantitative assessment of blood flow in the gastric conduit with thermal imaging for esophageal reconstruction. Ann Surg 271(6):1087–1094CrossRef Nishikawa K, Fujita T, Yuda M, Tanaka Y, Matsumoto A, Tanishima Y, Hanyu N, Yanaga K (2018) Quantitative assessment of blood flow in the gastric conduit with thermal imaging for esophageal reconstruction. Ann Surg 271(6):1087–1094CrossRef
30.
go back to reference Kitagawa H, Namikawa T, Iwabu J, Fujisawa K, Uemura S, Tsuda S, Hanazaki K (2018) Assessment of the blood supply using the indocyanine green fluorescence method and postoperative endoscopic evaluation of anastomosis of the gastric tube during esophagectomy. Surg Endosc 32:1749–1754CrossRef Kitagawa H, Namikawa T, Iwabu J, Fujisawa K, Uemura S, Tsuda S, Hanazaki K (2018) Assessment of the blood supply using the indocyanine green fluorescence method and postoperative endoscopic evaluation of anastomosis of the gastric tube during esophagectomy. Surg Endosc 32:1749–1754CrossRef
31.
go back to reference Kumagai Y, Hatano S, Sobajima J, Ishiguro T, Fukuchi M, Ishibashi K, Mochiki E, Nakajima Y, Ishida H (2018) Indocyanine green fluorescence angiography of the reconstructed gastric tube during esophagectomy: efficacy of the 90-second rule. Dis Esophagus 31:052 Kumagai Y, Hatano S, Sobajima J, Ishiguro T, Fukuchi M, Ishibashi K, Mochiki E, Nakajima Y, Ishida H (2018) Indocyanine green fluorescence angiography of the reconstructed gastric tube during esophagectomy: efficacy of the 90-second rule. Dis Esophagus 31:052
32.
go back to reference Ishige F, Nabeya Y, Hoshino I, Takayama W, Chiba S, Arimitsu H, Iwatate Y, Yanagibashi H (2019) Quantitative assessment of the blood perfusion of the gastric conduit by indocyanine green imaging. J Surg Res 234:303–310CrossRef Ishige F, Nabeya Y, Hoshino I, Takayama W, Chiba S, Arimitsu H, Iwatate Y, Yanagibashi H (2019) Quantitative assessment of the blood perfusion of the gastric conduit by indocyanine green imaging. J Surg Res 234:303–310CrossRef
33.
go back to reference Nerup N, Svendsen MBS, Svendsen LB, Achiam MP (2020) Feasibility and usability of real-time intraoperative quantitative fluorescent-guided perfusion assessment during resection of gastroesophageal junction cancer. Langenbeck's Arch Surg 405:1–8CrossRef Nerup N, Svendsen MBS, Svendsen LB, Achiam MP (2020) Feasibility and usability of real-time intraoperative quantitative fluorescent-guided perfusion assessment during resection of gastroesophageal junction cancer. Langenbeck's Arch Surg 405:1–8CrossRef
Metadata
Title
Quantitative serosal and mucosal optical imaging perfusion assessment in gastric conduits for esophageal surgery: an experimental study in enhanced reality
Authors
Manuel Barberio
Eric Felli
Margherita Pizzicannella
Vincent Agnus
Mahdi Al-Taher
Emilie Seyller
Yusef Moulla
Boris Jansen-Winkeln
Ines Gockel
Jacques Marescaux
Michele Diana
Publication date
01-10-2021
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 10/2021
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-020-08077-3

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