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

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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.

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References

  1. Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB (2019) Colorectal cancer. Lancet 394:1467–1480

    Article  Google Scholar 

  2. 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 68:394–424

    Article  Google Scholar 

  3. Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F (2017) Global patterns and trends in colorectal cancer incidence and mortality. Gut 66:683–691

    Article  Google Scholar 

  4. Races A, Males MWMB SEER Cancer Statistics Review 1975–2014

  5. 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 16:161–168

    Article  Google Scholar 

  6. Dahlberg M, Påhlman L, Bergström R, Glimelius B (1998) Improved survival in patients with rectal cancer: a population-based register study. Br J Surg 85:515–520

    Article  CAS  Google Scholar 

  7. 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 11:354–364

    Article  CAS  Google Scholar 

  8. 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 30:1763–1769

    Article  Google Scholar 

  9. 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 23:251–257

    Article  CAS  Google Scholar 

  10. 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 60:290–298

    Article  Google Scholar 

  11. 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 60:22–29

    Article  Google Scholar 

  12. 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 17:16

    Article  Google Scholar 

  13. Kim DH, Lubner MG, Cahoon AR, Pooler BD, Pickhardt PJ (2018) Flat serrated polyps at CT colonography: relevance, appearance, and optimizing interpretation. Radiographics 38:60–74

    Article  Google Scholar 

  14. 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 21:1151–1163

    Article  Google Scholar 

  15. 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 17:810–818

    Article  CAS  Google Scholar 

  16. Horton KM, Fishman EK (2010) CT angiography of the mesenteric circulation. Radiol Clin 48:331–345

    Article  Google Scholar 

  17. 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 27:2058–2067

    Article  Google Scholar 

  18. D'Agostino J, Diana M, Vix M, Soler L, Marescaux J (2012) Three-dimensional virtual neck exploration before parathyroidectomy. N Engl J Med 367:1072–1073

    Article  CAS  Google Scholar 

  19. 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 28:2493–2498

    Article  Google Scholar 

  20. 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 400:381–385

    Article  Google Scholar 

  21. 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 31:2863–2871

    Article  Google Scholar 

  22. 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 118:283–300

    Article  Google Scholar 

  23. Diana M (2018) Fluorescence-guided surgery applied to the digestive system: the cybernetic eye to see the invisible. Cir Esp 96:65–68

    Article  Google Scholar 

  24. 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 24:2921–2930

    Article  Google Scholar 

  25. Diana M (2017) Enabling precision digestive surgery with fluorescence imaging. Transl Gastroenterol Hepatol 2:97

    Article  Google Scholar 

  26. 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 30:2143–2150

    Article  Google Scholar 

  27. 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 28:321–325

    Article  Google Scholar 

  28. 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 12:561–563

    Article  Google Scholar 

  29. 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

    Google Scholar 

  30. 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 31:130–138

    Article  Google Scholar 

  31. 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 28:1432–1437

    Article  Google Scholar 

  32. 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 55:1063–1071

    Article  Google Scholar 

  33. Alander JT, Kaartinen I, Laakso A, Pätilä T, Spillmann T, Tuchin VV, Venermo M, Välisuo P (2012) A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging. https://doi.org/10.1155/2012/940585

    Article  PubMed  PubMed Central  Google Scholar 

  34. 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 8:4184

    Article  Google Scholar 

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Acknowledgments

The authors are grateful to Guy Temporal, professional in Medical English proofreading for his assistance with manuscript edition.

Funding

This study was partly funded by the IHU Strasbourg through the ANR Grant 10-IAHU-0002 and partly by the ARC Foundation for Cancer Research (9, rue Guy Môquet, BP 90003, 94803 Villejuif Cedex, France), via the ELIOS Grant (PI Michele Diana).

Author information

Authors and Affiliations

  1. Institute of Image-Guided Surgery, IHU Strasbourg, 1, place de l’Hôpital, 67091, Strasbourg, France

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

  2. IRCAD, Research Institute against Digestive Cancer, Strasbourg, France

    Jacques Marescaux & Michele Diana

  3. Department of General, Digestive, and Endocrine Surgery, University Hospital of Strasbourg, Strasbourg, France

    Michele Diana

  4. ICUBE Laboratory, Photonics Instrumentation for Health, Strasbourg, France

    Michele Diana

  5. University of Strasbourg, Strasbourg, France

    Benoit Gallix

  6. University Hospital of Strasbourg, Strasbourg, France

    Benoit Gallix

  7. Faculty of Medicine, McGill University, Montreal, Canada

    Benoit Gallix

Authors
  1. Antonello Forgione
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  2. Manuel Barberio
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  3. Vincent Agnus
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  4. Lee Swanström
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  5. Jacques Marescaux
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  6. Michele Diana
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  7. Benoit Gallix
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Corresponding author

Correspondence to Antonello Forgione.

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Disclosures

Michele Diana is member of the Scientific Board of Diagnostic Green. Michele Diana is the recipient of a grant from the ARC Foundation (https://www.fondation-arc.org/) for the ELIOS (Endoscopic Luminescent Imaging for precision Oncologic Surgery) project. Jacques Marescaux is the President of the IRCAD Institute, which is partly funded by KARL STORZ and Medtronic. Lee Swanström consults for Medtronic, Boston Scientific, and Olympus. Antonello Forgione, Manuel Barberio, Vincent Agnus, and Benoit Gallix have nothing to disclose.

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Forgione, A., Barberio, M., Agnus, V. et al. Precision image-guided colonic surgery: proof of concept for enhanced preoperative and intraoperative vascular imaging. Surg Endosc 35, 962–970 (2021). https://doi.org/10.1007/s00464-020-08000-w

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  • DOI: https://doi.org/10.1007/s00464-020-08000-w

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