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Simultaneous computer-assisted assessment of mucosal and serosal perfusion in a model of segmental colonic ischemia

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Abstract

Background

Fluorescence-based enhanced reality (FLER) enables the quantification of fluorescence signal dynamics, which can be superimposed onto real-time laparoscopic images by using a virtual perfusion cartogram. The current practice of perfusion assessment relies on visualizing the bowel serosa. The aim of this experimental study was to quantify potential differences in mucosal and serosal perfusion levels in an ischemic colon segment.

Methods

An ischemic colon segment was created in 12 pigs. Simultaneous quantitative mucosal and serosal fluorescence imaging was obtained via intravenous indocyanine green injection (0.2 mg/kg), using two near-infrared camera systems, and computer-assisted FLER analysis. Lactate levels were measured in capillary blood of the colonic wall at seven regions of interest (ROIs) as determined with FLER perfusion cartography: the ischemic zone (I), the proximal and distal vascularized areas (PV, DV), and the 50% perfusion threshold proximally and distally at the mucosal and serosal side (P50M, P50S, D50M, D50S).

Results

The mean ischemic zone as measured (mm) for the mucosal side was significantly larger than the serosal one (56.3 ± 21.3 vs. 40.8 ± 14.9, p = 0.001) with significantly lower lactate values at the mucosal ROIs. There was a significant weak inverse correlation between lactate and slope values for the defined ROIs (r = − 0.2452, p = 0.0246).

Conclusions

Mucosal ischemic zones were larger than serosal zones. These results suggest that an assessment of bowel perfusion from the serosal side only can underestimate the extent of ischemia. Further studies are required to predict the optimal resection margin and anastomotic site.

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References

  1. Seeliger B, Mascagni P, Longo F, Barberio M, Lapergola A, Mutter D, Klymchenko A, Agnus V, Marescaux J, Diana M (2019) Simultaneous computer-assisted assessment of mucosal and serosal perfusion in a model of segmental colonic ischemia. Br J Surg 106:19–19

    Google Scholar 

  2. Seeliger B, Barberio M, D’Urso A, Agnus V, Longo F, Mascagni P, Marescaux J, Mutter D, Diana M (2018) Fluorescence in rectal cancer surgery. Ann Laparosc Endosc Surg 3:47

    Article  Google Scholar 

  3. Hammond J, Lim S, Wan Y, Gao X, Patkar A (2014) The burden of gastrointestinal anastomotic leaks: an evaluation of clinical and economic outcomes. J Gastrointest Surg 18:1176–1185

    Article  Google Scholar 

  4. Cassinotti E, Costa S, DEP S, Oreggia B, Palazzini G, Boni L (2018) How to reduce surgical complications in rectal cancer surgery using fluorescence techniques. Minerva Chir 73:210–216

    PubMed  Google Scholar 

  5. 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 105:1359–1367

    Article  CAS  Google Scholar 

  6. Jafari MD, Wexner SD, Martz JE, McLemore EC, Margolin DA, Sherwinter DA, Lee SW, Senagore AJ, Phelan MJ, Stamos MJ (2015) Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR II): a multi-institutional study. J Am Coll Surg 220(82–92):e81

    Google Scholar 

  7. 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:e169–176

    Article  CAS  Google Scholar 

  8. Boni L, Fingerhut A, Marzorati A, Rausei S, Dionigi G, Cassinotti E (2017) Indocyanine green fluorescence angiography during laparoscopic low anterior resection: results of a case-matched study. Surg Endosc 31:1836–1840

    Article  Google Scholar 

  9. Karliczek A, Harlaar NJ, Zeebregts CJ, Wiggers T, Baas PC, van Dam GM (2009) Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Colorectal Dis 24:569–576

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  11. Mizrahi I, Abu-Gazala M, Rickles AS, Fernandez LM, Petrucci A, Wolf J, Sands DR, Wexner SD (2018) Indocyanine green fluorescence angiography during low anterior resection for low rectal cancer: results of a comparative cohort study. Tech Coloproctol 22:535–540

    Article  CAS  Google Scholar 

  12. 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 22:15–23

    Article  CAS  Google Scholar 

  13. Quero G, Lapergola A, Barberio M, Seeliger B, Gockel I, Saccomandi P, Guerriero L, Mutter D, Saadi A, Worreth M, Marescaux J, Agnus V, Diana M (2019) Discrimination between arterial and venous bowel ischemia by computer-assisted analysis of the fluorescent signal. Surg Endosc 33:1988–1997

    Article  Google Scholar 

  14. Singh DB, Stansby G, Bain I, Harrison DK (2009) Intraoperative measurement of colonic oxygenation during bowel resection. Adv Exp Med Biol 645:261–266

    Article  Google Scholar 

  15. Sherwinter DA (2012) Transanal near-infrared imaging of colorectal anastomotic perfusion. Surg Laparosc Endosc Percutan Tech 22:433–436

    Article  Google Scholar 

  16. Sherwinter DA, Gallagher J, Donkar T (2013) Intra-operative transanal near infrared imaging of colorectal anastomotic perfusion: a feasibility study. Colorectal Dis 15:91–96

    Article  CAS  Google Scholar 

  17. 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 28:3224–3233

    Article  Google Scholar 

  18. 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 28:3108–3118

    Article  Google Scholar 

  19. 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–e52

    Article  Google Scholar 

  20. 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 

  21. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8:e1000412

    Article  Google Scholar 

  22. Seeliger B, Walz MK, Alesina PF, Agnus V, Pop R, Barberio M, Saadi A, Worreth M, Marescaux J, Diana M (2019) Fluorescence-enabled assessment of adrenal gland localization and perfusion in posterior retroperitoneoscopic adrenal surgery in a preclinical model. Surg Endosc. https://doi.org/10.1007/s00464-019-06997-3

    Article  PubMed  PubMed Central  Google Scholar 

  23. Oliphant TE (2007) Python for scientific computing. Comput Sci Eng 9:10–20

    Article  CAS  Google Scholar 

  24. Alemanno G, Somigli R, Prosperi P, Bergamini C, Maltinti G, Giordano A, Valeri A (2016) Combination of diagnostic laparoscopy and intraoperative indocyanine green fluorescence angiography for the early detection of intestinal ischemia not detectable at CT scan. Int J Surg Case Rep 26:77–80

    Article  Google Scholar 

  25. Vollmar B, Menger MD (2011) Intestinal ischemia/reperfusion: microcirculatory pathology and functional consequences. Langenbecks Arch Surg 396:13–29

    Article  Google Scholar 

  26. Hogberg N, Carlsson PO, Hillered L, Meurling S, Stenback A (2012) Intestinal ischemia measured by intraluminal microdialysis. Scand J Clin Lab Invest 72:59–66

    Article  Google Scholar 

  27. 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 3:59–69

    Article  Google Scholar 

  28. Grootjans J, Lenaerts K, Buurman WA, Dejong CH, Derikx JP (2016) Life and death at the mucosal-luminal interface: new perspectives on human intestinal ischemia-reperfusion. World J Gastroenterol 22:2760–2770

    Article  CAS  Google Scholar 

  29. Grone J, Koch D, Kreis ME (2015) Impact of intraoperative microperfusion assessment with pinpoint perfusion imaging on surgical management of laparoscopic low rectal and anorectal anastomoses. Colorectal Dis 17(Suppl 3):22–28

    Article  Google Scholar 

  30. Al Furajii H, Cahill RA (2015) Laparoscopic and Endoscopic Near-infrared Perfusion Assessment of in situ ileoileal, ileocolic, colocolic, colorectal and ileoanal anastomosis during intestinal operation for benign and malignant disease: a Video Vignette. Colorectal Dis 17(Suppl 3):37

    Article  Google Scholar 

  31. Guraieb-Trueba M, Frering T, Atallah S (2016) Combined endoscopic and laparoscopic real-time intra-operative evaluation of bowel perfusion using fluorescence angiography. Tech Coloproctol 20:883–884

    Article  CAS  Google Scholar 

  32. 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 22:453–461

    Article  Google Scholar 

  33. Mascagni P, Longo F, Barberio M, Seeliger B, Agnus V, Saccomandi P, Hostettler A, Marescaux J, Diana M (2018) New intraoperative imaging technologies: innovating the surgeon’s eye toward surgical precision. J Surg Oncol 118:265–282

    Article  Google Scholar 

  34. Son GM, Kwon MS, Kim Y, Kim J, Kim SH, Lee JW (2019) Quantitative analysis of colon perfusion pattern using indocyanine green (ICG) angiography in laparoscopic colorectal surgery. Surg Endosc 33:1640–1649

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank Renée Geraats, Marinka Oudkerk Pool, and Julian Abbing for technical and operative assistance. The authors are also grateful to Camille Goustiaux, Christopher Burel, and Guy Temporal for their assistance in proofreading the manuscript. The TEO®/laparoscopic equipment for this study has been kindly supplied by KARL STORZ SE & Co. KG.

Funding

This study was funded by the ARC Foundation (www.fondation-arc.org).

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Authors and Affiliations

  1. IHU-Strasbourg Institute of Image-Guided Surgery, Strasbourg, France

    Barbara Seeliger, Vincent Agnus, Pietro Mascagni, Manuel Barberio, Fabio Longo, Alfonso Lapergola, Didier Mutter, Jacques Marescaux & Michele Diana

  2. Institute for Research Against Cancer of the Digestive System (IRCAD), Strasbourg, France

    Barbara Seeliger, Didier Mutter, Jacques Marescaux & Michele Diana

  3. Department of General, Digestive and Endocrine Surgery, University Hospital of Strasbourg, 1, place de l’Hôpital, 67091, Strasbourg Cedex, France

    Didier Mutter & Michele Diana

  4. Faculty of Pharmacy, Nanochemistry and Bioimaging Laboratory, UMR 7021, CNRS, University of Strasbourg, Strasbourg, France

    Andrey S. Klymchenko

  5. Division of Surgery and Interventional Sciences, University College London, London, UK

    Manish Chand

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  1. Barbara Seeliger
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  2. Vincent Agnus
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  4. Manuel Barberio
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  9. Manish Chand
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  10. Jacques Marescaux
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  11. Michele Diana
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Corresponding author

Correspondence to Michele Diana.

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Disclosures

Michele Diana is the recipient of the ELIOS grant from the ARC Foundation. Michele Diana and Andrey Klymchenko report a European patent application filed (no. 18305075.6) under the title “NIR fluorescent polymer coating”. Jacques Marescaux is the President of both IRCAD and IHU-Strasbourg Institutes, which are partly funded by KARL STORZ, Medtronic, and Siemens Healthcare. Manish Chand reports consultancy fees for teaching for Stryker. Barbara Seeliger, Vincent Agnus, Pietro Mascagni, Manuel Barberio, Fabio Longo, Alfonso Lapergola, and Didier Mutter have no conflicts of interest or financial ties to disclose.

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Seeliger, B., Agnus, V., Mascagni, P. et al. Simultaneous computer-assisted assessment of mucosal and serosal perfusion in a model of segmental colonic ischemia. Surg Endosc 34, 4818–4827 (2020). https://doi.org/10.1007/s00464-019-07258-z

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  • DOI: https://doi.org/10.1007/s00464-019-07258-z

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