Skip to main content
Top
Published in: Surgical Endoscopy 2/2021

01-02-2021 | Dynamic Manuscript

Precision image-guided colonic surgery: proof of concept for enhanced preoperative and intraoperative vascular imaging

Authors: Antonello Forgione, Manuel Barberio, Vincent Agnus, Lee Swanström, Jacques Marescaux, Michele Diana, Benoit Gallix

Published in: Surgical Endoscopy | Issue 2/2021

Login to get access

Abstract

Background

Colorectal surgery has benefited from advances in precision medicine such as total mesorectal resection, and recently, mesocolon resection, fluorescent perfusion imaging, and fluorescent node mapping. However, these advances fail to address the variable quality of mesocolon dissection and the directed extent of vascular dissection (including high ligation) or pre-resection anastomotic perfusion mapping, thereby impacting anastomotic leaks. We propose a new paradigm of precision image-directed colorectal surgery involving 3D preoperative resection modeling and intraoperative fluoroscopic and fluorescence vascular imaging which better defines optimal dissection planes and vascular vs. anatomy-based resection lines according to our hypothesis.

Methods

Six pigs had preoperative CT with vascular 3D reconstruction allowing for the preoperative planning of vascular-based dissection. Laparoscopic surgery was performed in a hybrid operating room (OR). Superselective arterial catheterization was performed in branches of the superior mesenteric artery (SMA) or the inferior mesenteric artery (IMA). Intraoperative boluses of 0.1 mg/kg or a continuous infusion of indocyanine green (ICG) (0.01 mg/mL) were administered to guide fluorescent-based sigmoid and ileocecal resections. Fluorescence was assessed using proprietary software at several regions of interest (ROI) in the right and left colon.

Results

The approach was feasible and safe. Selective catheterization took an average of 43 min. Both bolus and continuous perfusion clearly marked pre-identified vessels (arteries/veins) and the target colon segment, facilitating precise resections based on the visible vascular anatomy. Quantitative software analysis indicated the optimal resection margin for each ROI.

Conclusion

Intra-arterial fluorescent mapping allows visualization of major vascular structures and segmental colonic perfusion. This may help to prevent any inadvertent injury to major vascular structures and to precisely determine perfusion-based resection planes and margins. This could enable tailoring of the amount of colon resected, ensure good anastomotic perfusion, and improve oncological outcomes.
Appendix
Available only for authorised users
Literature
1.
go back to reference Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB (2019) Colorectal cancer. Lancet 394:1467–1480CrossRef Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB (2019) Colorectal cancer. Lancet 394:1467–1480CrossRef
2.
go back to reference Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424CrossRef Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424CrossRef
3.
go back to reference Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F (2017) Global patterns and trends in colorectal cancer incidence and mortality. Gut 66:683–691CrossRef Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F (2017) Global patterns and trends in colorectal cancer incidence and mortality. Gut 66:683–691CrossRef
4.
go back to reference Races A, Males MWMB SEER Cancer Statistics Review 1975–2014 Races A, Males MWMB SEER Cancer Statistics Review 1975–2014
5.
go back to reference Bertelsen CA, Neuenschwander AU, Jansen JE, Wilhelmsen M, Kirkegaard-Klitbo A, Tenma JR, Bols B, Ingeholm P, Rasmussen LA, Jepsen LV, Iversen ER, Kristensen B, Gogenur I, Danish Colorectal Cancer G (2015) Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: a retrospective, population-based study. Lancet Oncol 16:161–168CrossRef Bertelsen CA, Neuenschwander AU, Jansen JE, Wilhelmsen M, Kirkegaard-Klitbo A, Tenma JR, Bols B, Ingeholm P, Rasmussen LA, Jepsen LV, Iversen ER, Kristensen B, Gogenur I, Danish Colorectal Cancer G (2015) Disease-free survival after complete mesocolic excision compared with conventional colon cancer surgery: a retrospective, population-based study. Lancet Oncol 16:161–168CrossRef
6.
go back to reference Dahlberg M, Påhlman L, Bergström R, Glimelius B (1998) Improved survival in patients with rectal cancer: a population-based register study. Br J Surg 85:515–520CrossRef Dahlberg M, Påhlman L, Bergström R, Glimelius B (1998) Improved survival in patients with rectal cancer: a population-based register study. Br J Surg 85:515–520CrossRef
7.
go back to reference Hohenberger W, Weber K, Matzel K, Papadopoulos T, Merkel S (2009) Standardized surgery for colonic cancer: complete mesocolic excision and central ligation–technical notes and outcome. Colorectal Dis 11:354–364CrossRef Hohenberger W, Weber K, Matzel K, Papadopoulos T, Merkel S (2009) Standardized surgery for colonic cancer: complete mesocolic excision and central ligation–technical notes and outcome. Colorectal Dis 11:354–364CrossRef
8.
go back to reference West NP, Kobayashi H, Takahashi K, Perrakis A, Weber K, Hohenberger W, Sugihara K, Quirke P (2012) Understanding optimal colonic cancer surgery: comparison of Japanese D3 resection and European complete mesocolic excision with central vascular ligation. J Clin Oncol 30:1763–1769CrossRef West NP, Kobayashi H, Takahashi K, Perrakis A, Weber K, Hohenberger W, Sugihara K, Quirke P (2012) Understanding optimal colonic cancer surgery: comparison of Japanese D3 resection and European complete mesocolic excision with central vascular ligation. J Clin Oncol 30:1763–1769CrossRef
9.
go back to reference Benz S, Tannapfel A, Tam Y, Grünenwald A, Vollmer S, Stricker I (2019) Proposal of a new classification system for complete mesocolic excison in right-sided colon cancer. Tech Coloproctol 23:251–257CrossRef Benz S, Tannapfel A, Tam Y, Grünenwald A, Vollmer S, Stricker I (2019) Proposal of a new classification system for complete mesocolic excison in right-sided colon cancer. Tech Coloproctol 23:251–257CrossRef
10.
go back to reference Kuzu MA, Ismail E, Çelik S, Şahin MF, Güner MA, Hohenberger W, Açar HI (2017) Variations in the vascular anatomy of the right colon and implications for right-sided colon surgery. Dis Colon Rectum 60:290–298CrossRef Kuzu MA, Ismail E, Çelik S, Şahin MF, Güner MA, Hohenberger W, Açar HI (2017) Variations in the vascular anatomy of the right colon and implications for right-sided colon surgery. Dis Colon Rectum 60:290–298CrossRef
11.
go back to reference Alsabilah JF, Razvi SA, Albandar MH, Kim NK (2017) Intraoperative archive of right colonic vascular variability aids central vascular ligation and redefines gastrocolic trunk of henle variants. Dis Colon Rectum 60:22–29CrossRef Alsabilah JF, Razvi SA, Albandar MH, Kim NK (2017) Intraoperative archive of right colonic vascular variability aids central vascular ligation and redefines gastrocolic trunk of henle variants. Dis Colon Rectum 60:22–29CrossRef
12.
go back to reference Wu C, Ye K, Wu Y, Chen Q, Xu J, Lin J, Kang W (2019) Variations in right colic vascular anatomy observed during laparoscopic right colectomy. World J Surg Oncol 17:16CrossRef Wu C, Ye K, Wu Y, Chen Q, Xu J, Lin J, Kang W (2019) Variations in right colic vascular anatomy observed during laparoscopic right colectomy. World J Surg Oncol 17:16CrossRef
13.
go back to reference Kim DH, Lubner MG, Cahoon AR, Pooler BD, Pickhardt PJ (2018) Flat serrated polyps at CT colonography: relevance, appearance, and optimizing interpretation. Radiographics 38:60–74CrossRef Kim DH, Lubner MG, Cahoon AR, Pooler BD, Pickhardt PJ (2018) Flat serrated polyps at CT colonography: relevance, appearance, and optimizing interpretation. Radiographics 38:60–74CrossRef
14.
go back to reference Maupoey Ibáñez J, Pàmies Guilabert J, Frasson M, Boscà Robledo A, Giner Segura F, García-Granero Ximénez E (2019) Accuracy of CT-Colonography in the preoperative staging of colon cancer. A prospective study of 217 patients. Colorectal Dis 21:1151–1163CrossRef Maupoey Ibáñez J, Pàmies Guilabert J, Frasson M, Boscà Robledo A, Giner Segura F, García-Granero Ximénez E (2019) Accuracy of CT-Colonography in the preoperative staging of colon cancer. A prospective study of 217 patients. Colorectal Dis 21:1151–1163CrossRef
15.
go back to reference Nesgaard J, Stimec B, Bakka A, Edwin B, Ignjatovic D, Group RS, Oresland T, Færden AE, Thorsen Y, Andersen S (2015) Navigating the mesentery: a comparative pre-and per-operative visualization of the vascular anatomy. Colorectal Dis 17:810–818CrossRef Nesgaard J, Stimec B, Bakka A, Edwin B, Ignjatovic D, Group RS, Oresland T, Færden AE, Thorsen Y, Andersen S (2015) Navigating the mesentery: a comparative pre-and per-operative visualization of the vascular anatomy. Colorectal Dis 17:810–818CrossRef
16.
go back to reference Horton KM, Fishman EK (2010) CT angiography of the mesenteric circulation. Radiol Clin 48:331–345CrossRef Horton KM, Fishman EK (2010) CT angiography of the mesenteric circulation. Radiol Clin 48:331–345CrossRef
17.
go back to reference Mari FS, Nigri G, Pancaldi A, De Cecco CN, Gasparrini M, Dall’Oglio A, Pindozzi F, Laghi A, Brescia A (2013) Role of CT angiography with three-dimensional reconstruction of mesenteric vessels in laparoscopic colorectal resections: a randomized controlled trial. Surg Endosc 27:2058–2067CrossRef Mari FS, Nigri G, Pancaldi A, De Cecco CN, Gasparrini M, Dall’Oglio A, Pindozzi F, Laghi A, Brescia A (2013) Role of CT angiography with three-dimensional reconstruction of mesenteric vessels in laparoscopic colorectal resections: a randomized controlled trial. Surg Endosc 27:2058–2067CrossRef
18.
go back to reference D'Agostino J, Diana M, Vix M, Soler L, Marescaux J (2012) Three-dimensional virtual neck exploration before parathyroidectomy. N Engl J Med 367:1072–1073CrossRef D'Agostino J, Diana M, Vix M, Soler L, Marescaux J (2012) Three-dimensional virtual neck exploration before parathyroidectomy. N Engl J Med 367:1072–1073CrossRef
19.
go back to reference Pessaux P, Diana M, Soler L, Piardi T, Mutter D, Marescaux J (2014) Robotic duodenopancreatectomy assisted with augmented reality and real-time fluorescence guidance. Surg Endosc 28:2493–2498CrossRef Pessaux P, Diana M, Soler L, Piardi T, Mutter D, Marescaux J (2014) Robotic duodenopancreatectomy assisted with augmented reality and real-time fluorescence guidance. Surg Endosc 28:2493–2498CrossRef
20.
go back to reference Pessaux P, Diana M, Soler L, Piardi T, Mutter D, Marescaux J (2015) Towards cybernetic surgery: robotic and augmented reality-assisted liver segmentectomy. Langenb Arch Surg 400:381–385CrossRef Pessaux P, Diana M, Soler L, Piardi T, Mutter D, Marescaux J (2015) Towards cybernetic surgery: robotic and augmented reality-assisted liver segmentectomy. Langenb Arch Surg 400:381–385CrossRef
21.
go back to reference Kong S-H, Haouchine N, Soares R, Klymchenko A, Andreiuk B, Marques B, Shabat G, Piéchaud T, Diana M, Cotin S (2017) Robust augmented reality registration method for localization of solid organs’ tumors using CT-derived virtual biomechanical model and fluorescent fiducials. Surg Endosc 31:2863–2871CrossRef Kong S-H, Haouchine N, Soares R, Klymchenko A, Andreiuk B, Marques B, Shabat G, Piéchaud T, Diana M, Cotin S (2017) Robust augmented reality registration method for localization of solid organs’ tumors using CT-derived virtual biomechanical model and fluorescent fiducials. Surg Endosc 31:2863–2871CrossRef
22.
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 118:283–300CrossRef 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 118:283–300CrossRef
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 96:65–68CrossRef Diana M (2018) Fluorescence-guided surgery applied to the digestive system: the cybernetic eye to see the invisible. Cir Esp 96:65–68CrossRef
24.
go back to reference 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 24:2921–2930CrossRef 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 24:2921–2930CrossRef
25.
go back to reference Diana M (2017) Enabling precision digestive surgery with fluorescence imaging. Transl Gastroenterol Hepatol 2:97CrossRef Diana M (2017) Enabling precision digestive surgery with fluorescence imaging. Transl Gastroenterol Hepatol 2:97CrossRef
26.
go back to reference Liu Y-Y, Pop R, Diana M, Kong S-H, Lègner A, Beaujeux R, Marescaux J (2016) Real-time fluorescence angiography by intra-arterial indocyanine green injection to identify obscure gastrointestinal bleeding territory: proof of concept in the porcine model. Surg Endosc 30:2143–2150CrossRef Liu Y-Y, Pop R, Diana M, Kong S-H, Lègner A, Beaujeux R, Marescaux J (2016) Real-time fluorescence angiography by intra-arterial indocyanine green injection to identify obscure gastrointestinal bleeding territory: proof of concept in the porcine model. Surg Endosc 30:2143–2150CrossRef
27.
go back to reference Heiliger C, Piecuch J, Frank A, Andrade D, Von Ehrlich-Treuenstätt V, Schiergens T, Rentsch M, Werner J, Karcz K (2018) Intraarterial indocyanine green (ICG) fluorescence augmentation by marking embryonal resection areas in colorectal surgery: a feasibility study in a porcine model. Minim Invasive Ther Allied Technol 28:321–325CrossRef Heiliger C, Piecuch J, Frank A, Andrade D, Von Ehrlich-Treuenstätt V, Schiergens T, Rentsch M, Werner J, Karcz K (2018) Intraarterial indocyanine green (ICG) fluorescence augmentation by marking embryonal resection areas in colorectal surgery: a feasibility study in a porcine model. Minim Invasive Ther Allied Technol 28:321–325CrossRef
28.
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
29.
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
30.
go back to reference van Dijk LJ, van Noord D, van Mierlo M, Bijdevaate DC, Bruno MJ, Moelker A (2020) Single-center retrospective comparative analysis of transradial, transbrachial, and transfemoral approach for mesenteric arterial procedures. J Vasc Interv Radiol 31:130–138CrossRef van Dijk LJ, van Noord D, van Mierlo M, Bijdevaate DC, Bruno MJ, Moelker A (2020) Single-center retrospective comparative analysis of transradial, transbrachial, and transfemoral approach for mesenteric arterial procedures. J Vasc Interv Radiol 31:130–138CrossRef
31.
go back to reference Khalilzadeh O, Baerlocher MO, Shyn PB, Connolly BL, Devane AM, Morris CS, Cohen AM, Midia M, Thornton RH, Gross K (2017) Proposal of a new adverse event classification by the Society of Interventional Radiology Standards of Practice Committee. J Vasc Interv Radiol 28:1432–1437CrossRef Khalilzadeh O, Baerlocher MO, Shyn PB, Connolly BL, Devane AM, Morris CS, Cohen AM, Midia M, Thornton RH, Gross K (2017) Proposal of a new adverse event classification by the Society of Interventional Radiology Standards of Practice Committee. J Vasc Interv Radiol 28:1432–1437CrossRef
32.
go back to reference Oderich GS, Tallarita T, Gloviczki P, Duncan AA, Kalra M, Misra S, Cha S, Bower TC (2012) Mesenteric artery complications during angioplasty and stent placement for atherosclerotic chronic mesenteric ischemia. J Vasc Surg 55:1063–1071CrossRef Oderich GS, Tallarita T, Gloviczki P, Duncan AA, Kalra M, Misra S, Cha S, Bower TC (2012) Mesenteric artery complications during angioplasty and stent placement for atherosclerotic chronic mesenteric ischemia. J Vasc Surg 55:1063–1071CrossRef
34.
go back to reference Negoi I, Beuran M, Hostiuc S, Negoi RI, Inoue Y (2018) Surgical anatomy of the superior mesenteric vessels related to colon and pancreatic surgery: a systematic review and meta-analysis. Sci Rep 8:4184CrossRef Negoi I, Beuran M, Hostiuc S, Negoi RI, Inoue Y (2018) Surgical anatomy of the superior mesenteric vessels related to colon and pancreatic surgery: a systematic review and meta-analysis. Sci Rep 8:4184CrossRef
Metadata
Title
Precision image-guided colonic surgery: proof of concept for enhanced preoperative and intraoperative vascular imaging
Authors
Antonello Forgione
Manuel Barberio
Vincent Agnus
Lee Swanström
Jacques Marescaux
Michele Diana
Benoit Gallix
Publication date
01-02-2021
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 2/2021
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-020-08000-w

Other articles of this Issue 2/2021

Surgical Endoscopy 2/2021 Go to the issue