Indocyanine green-enhanced fluorescence to assess bowel perfusion during laparoscopic colorectal resection

Luigi Boni, Giulia David, Gianlorenzo Dionigi, Stefano Rausei, Elisa Cassinotti, Abe Fingerhut, Luigi Boni, Giulia David, Gianlorenzo Dionigi, Stefano Rausei, Elisa Cassinotti, Abe Fingerhut

Abstract

Aims: Anastomotic leakage after colorectal surgery is a severe complication. One possible cause of anastomotic leakage is insufficient vascular supply. The aim of this study was to evaluate the feasibility and the usefulness of intraoperative assessment of vascular anastomotic perfusion in colorectal surgery using indocyanine green (ICG)-enhanced fluorescence.

Methods: Between May 2013 and October 2014, all anastomosis and resection margins in colorectal surgery were investigated using fluorescence angiography (KARL STORZ GmbH & Co. KG, Tuttlingen, Germany) intraoperatively to assess colonic perfusion prior to and after completion of the anastomosis, both in right and left colectomies.

Results: A total of 107 patients undergoing colorectal laparoscopic resections were enrolled: 40 right colectomies, 10 splenic flexure segmental resections, 35 left colectomies, and 22 anterior resections. In 90 % of cases, the indication for surgery was cancer and high ligation of vessels was performed. Based on the fluorescence intensity, the surgical team judged the distal part of the proximal bowel to be anastomosed insufficiently perfused in 4/107 patients (two anterior, one sigmoid and one segmental splenic flexure resections for cancer), and consequently, further proximal "re-resection" up to a "fluorescent" portion was performed. None of these patients had a clinical leak. The overall morbidity rate was 30 %; one patient undergoing right colectomy had an anastomotic leakage, apparently unrelated to ischemia; there were no clinical evident anastomotic leakages in colorectal resections including all low anterior resections.

Conclusions: ICG-enhanced fluorescent angiography provides useful intraoperative information about the vascular perfusion during colorectal surgery and may lead to change the site of resection and/or anastomosis, possibly affecting the anastomotic leak rate. Larger further randomized prospective trials are needed to validate this new technique.

Keywords: Anastomotic leaks; Bowel perfusion; Colorectal resection; Fluorescence; ICG; Indocyanine green.

Figures

Fig. 1
Fig. 1
Intraoperative view of the descending colon after division of the mesentery: Surgical clip is placed at the point of planned transection (A view with standard light, B view with NIR light showing good perfusion)
Fig. 2
Fig. 2
Intraoperative view of the descending colon in a case of hypoperfusion at the point of planned transection (arrows)

References

    1. Buchs NC, Gervaz P, Secic M, Bucher P, Mugnier-Konrad B, Morel P. Incidence, consequences, and risk factors for anastomotic dehiscence after colorectal surgery: a prospective monocentric study. Int J Colorectal Dis. 2008;23(3):265–270. doi: 10.1007/s00384-007-0399-3.
    1. Mirnezami A, Mirnezami R, Chandrakumaran K, Sasapu K, Sagar P, Finan P. Increased local recurrence and reduced survival from colorectal cancer following anastomotic leak: systematic review and meta-analysis. Ann Surg. 2011;253(5):890–899. doi: 10.1097/SLA.0b013e3182128929.
    1. Park JS, Choi GS, Kim SH, Kim HR, Kim NK, Lee KY, Kang SB, Kim JY, Lee KY, Kim BC, Bae BN, Son GM, Lee SI, Kang H. Multicenter analysis of risk factors for anastomotic leakage after laparoscopic rectal cancer excision: the Korean laparoscopic colorectal surgery study group. Ann Surg. 2013;257(4):665–671. doi: 10.1097/SLA.0b013e31827b8ed9.
    1. Alves A, Panis Y, Pocard M, Regimbeau JM, Valleur P. Management of anastomotic leakage after nondiverted large bowel resection. J Am Coll Surg. 1999;189(6):554–559. doi: 10.1016/S1072-7515(99)00207-0.
    1. Nesbakken A, Nygaard K, Westerheim O, Lunde OC, Mala T. Audit of intraoperative and early postoperative complications after introduction of mesorectal excision for rectal cancer. Eur J Surg. 2002;168(4):229–235. doi: 10.1080/11024150260102843.
    1. Al Asari S, Cho MS, Kim NK. Safe anastomosis in laparoscopic and robotic low anterior resection for rectal cancer: a narrative review and outcomes study from an expert tertiary center. Eur J Surg Oncol. 2015;41(2):175–185. doi: 10.1016/j.ejso.2014.10.060.
    1. Shogan BD, Carlisle EM, Alverdy JC, Umanskiy K. Do we really know why colorectal anastomoses leak? J Gastrointest Surg. 2013;17(9):1698–1707. doi: 10.1007/s11605-013-2227-0.
    1. Frasson M, Flor-Lorente B, Ramos Rodríguez JL, Granero-Castro P, Hervás D, Alvarez Rico MA, Brao MJ, Sánchez González JM, Garcia-Granero E, ANACO Study Group; ANACO Study Group Risk factors for anastomotic leak after colon resection for cancer: multivariate analysis and nomogram from a multicentric, prospective, national study with 3193 patients. Ann Surg. 2015;262(2):321–330. doi: 10.1097/SLA.0000000000000973.
    1. Kingham TP, Pachter HL. Colonic anastomotic leak: risk factors, diagnosis, and treatment. J Am Coll Surg. 2009;208(2):269–278. doi: 10.1016/j.jamcollsurg.2008.10.015.
    1. Karliczek A, Harlaar NJ, Zeebregts CJ, Wiggers T, Baas PC, Van Dam GM. Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Colorectal Dis. 2009;24(5):569–576. doi: 10.1007/s00384-009-0658-6.
    1. Markus PM, Martell J, Leister I, Horstmann O, Brinker J, Becker H. Predicting postoperative morbidity by clinical assessment. Br J Surg. 2005;92:101–106. doi: 10.1002/bjs.4608.
    1. Luo S, Zhang E, Su Y, Cheng T, Shi C. A review of NIR dyes in cancer targeting and imaging. Biomaterials. 2011;32:7127–7138. doi: 10.1016/j.biomaterials.2011.06.024.
    1. Boni L, David G, Mangano A, Dionigi G, Rausei S, Spampatti S, Cassinotti E, Fingerhut A. Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc. 2014
    1. Liu DZ, Mathes DW, Zenn MR, Neligan PC. The application of indocyanine green fluorescence angiography in plastic surgery. J Reconstr Microsurg. 2014;27(6):355–364. doi: 10.1055/s-0031-1281515.
    1. Arichi N, Mitsui Y, Ogawa K, Nagami T, Nakamura S, Hiraoka T, Yasumoto H, Shiina H. Intraoperative fluorescence vascular Imaging using indocyanine green for assessment of transplanted kidney perfusion. Transplant. 2014;46:342–345. doi: 10.1016/j.transproceed.2013.11.129.
    1. Zehetner J, DeMeester SR, Alicuben ET, Oh DS, Lipham JC, Hagen JA, DeMeester TR. Intraoperative assessment of perfusion of the gastric graft and correlation with anastomotic leaks after esophagectomy. Ann Surg. 2014
    1. Jafari MD, Wexner SD, Martz JE, McLemore EC, Margolin DA, Sherwinter DA, Lee SW, Senagore AJ, Phelan MJ, Stamos MJ. Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR II): a multi-institutional study. J Am Coll Surg. 2015;220(1):82–92.e1. doi: 10.1016/j.jamcollsurg.2014.09.015.
    1. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibanes Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron J, Makuchi M. The Clavien-Dindo classification of surgical complications five-year experience. Ann Surg. 2009;250:187–196. doi: 10.1097/SLA.0b013e3181b13ca2.
    1. Daams F, Wu Z, Lahaye MJ, Jeekel J, Lange JF. Prediction and diagnosis of colorectal anastomotic leakage: a systematic review of literature. World J Gastrointest Surg. 2014;6(2):14–26. doi: 10.4240/wjgs.v6.i2.14.
    1. Ambrosetti P, Robert J, Mathey P, Rohner A. Left-sided colon and colorectal anastomoses: doppler ultrasound as an aid to assess bowel vascularization. A prospective evaluation of 200 consecutive elective cases. Int J Colorectal Dis. 1994;9(4):211–214. doi: 10.1007/BF00292253.
    1. Boyle NH, Manifold D, Jordan MH, Mason RC. Intraoperative assessment of colonic perfusion using scanning laser Doppler flowmetry during colonic resection. J Am Coll Surg. 2000;191(5):504–510. doi: 10.1016/S1072-7515(00)00709-2.
    1. Karliczek A, Benaron DA, Baas PC, Zeebregts CJ, Wiggers T, van Dam GM. Intraoperative assessment of microperfusion with visible light spectroscopy for prediction of anastomotic leakage in colorectal anastomoses. Colorectal Dis. 2010;12(10):1018–1025. doi: 10.1111/j.1463-1318.2009.01944.x.
    1. Vignali A, Gianotti L, Braga M, Radaelli G, Malvezzi L, Di Carlo V. Altered microperfusion at the rectal stump is predictive for rectal anastomotic leak. Dis Colon Rectum. 2000;43(1):76–82. doi: 10.1007/BF02237248.
    1. Kudszus S, Roesel C, Schachtrupp A, Höer JJ. Intraoperative laser fluorescence angiography in colorectal surgery: a noninvasive analysis to reduce the rate of anastomotic leakage. Langenbecks Arch Surg. 2010;395(8):1025–1030. doi: 10.1007/s00423-010-0699-x.
    1. Jafari MD, Lee KH, Halabi WJ, Mills SD, Carmichael JC, Stamos MJ, Pigazzi A. The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc. 2013;27(8):3003–3008. doi: 10.1007/s00464-013-2832-8.
    1. Pigazzi A, Luca F, Patriti A, Valvo M, Ceccarelli G, Casciola L, Biffi R, Garcia-Aguilar J, Baek JH. Multicentric study on robotic tumor-specific mesorectal excision for the treatment of rectal cancer. Ann Surg Oncol. 2010;17(6):1614–1620. doi: 10.1245/s10434-010-0909-3.
    1. Kin C, Vo H, Welton L, Welton M. Equivocal effect of intraoperative fluorescence angiography on colorectal anastomotic leaks. Dis Colon Rectum. 2015;58(6):582–587. doi: 10.1097/DCR.0000000000000320.
    1. Sheridan WG, Lowndes RH, Young HL. Tissue oxygen tension as a predictor of colonic anastomotic healing. Dis Colon Rectum. 1987;30:867. doi: 10.1007/BF02555426.
    1. Al-Asari SF, Lim D, Min BS, Kim NK. The relation between inferior mesenteric vein ligation and collateral vessels to splenic flexure: anatomical landmarks, technical precautions and clinical significance. Yonsei Med J. 2013;54(6):1484–1490. doi: 10.3349/ymj.2013.54.6.1484.
    1. Titu LV, Tweedle E, Rooney PS. High tie of the inferior mesenteric artery in curative surgery for left colonic and rectal cancers: a systematic review. Dig Surg. 2008;25(2):148–157. doi: 10.1159/000128172.
    1. Golligher JC. The adequacy of the marginal blood supply to the left colon after high ligation of the inferior mesenteric artery during excision of the rectum. Br J Surg. 1954;41:351–353. doi: 10.1002/bjs.18004116804.
    1. Griffiths JD. Surgical anatomy of the blood supply of the distal colon. Ann R Coll Surg Engl. 1956;19:241–256.
    1. Sakorafas GH, Zouros E, Peros G. Applied vascular anatomy of the colon and rectum: clinical implications for the surgical oncologist. Surg Oncol. 2006;15(4):243–255. doi: 10.1016/j.suronc.2007.03.002.
    1. Trencheva K, Morrissey KP, Wells M, Mancuso CA, Lee SW, Sonoda T, Michelassi F, Charlson ME, Milsom JW. Identifying important predictors for anastomotic leak after colon and rectal resection prospective study on 616 patients. Ann Surg. 2013;257:108–113. doi: 10.1097/SLA.0b013e318262a6cd.
    1. Hellan M, Spinoglio G, Pigazzi A, Lagares-Garcia JA. The influence of fluorescence imaging on the location of bowel transection during robotic left-sided colorectal surgery. Surg Endosc. 2014;28(5):1695–1702. doi: 10.1007/s00464-013-3377-6.
    1. Alves A, Panis Y, Trancart D, Regimbeau JM, Pocard M, Valleur P. Factors associated with clinically significant anastomotic leakage after large bowel resection: multivariate analysis of 707 patients. World J Surg. 2002;26(4):499–502. doi: 10.1007/s00268-001-0256-4.
    1. Leather RP, Shah DM, Kaufman JL. Comparative analysis of retroperitoneal and transperitoneal aortic replacement for aneurysm. Surg Gynecol Obstet. 1989;168:38–41.
    1. Verbeek FP, Schaafsma BE, Tummers QR, van der Vorst JR, van der Made WJ, Baeten CI, Bonsing BA, Frangioni JV, van de Velde CJ, Vahrmeijer AL, Swijnenburg RJ. Optimization of near-infrared fluorescence cholangiography for open and laparoscopic surgery. Surg Endosc. 2014;28:1076–1082. doi: 10.1007/s00464-013-3305-9.
    1. Diana M, Halvax P, Dallemagne B, Nagao Y, Diemunsch P, Charles AL, Agnus V, Soler L, Demartines N, Lindner V, Geny B, Marescaux J. Real-time navigation by fluorescence-based enhanced reality for precise estimation of future anastomotic site in digestive surgery. Surg Endosc. 2014;28:3108–3118. doi: 10.1007/s00464-014-3592-9.
    1. Diana M, Agnus V, Halvax P, Liu YY, Dallemagne B, Schlagowski AI, Geny B, Diemunsch P, Lindner V, Marescaux J. Intraoperative fluorescence-based enhanced reality laparoscopic real-time imaging to assess bowel perfusion at the anastomotic site in an experimental model. Br J Surg. 2015;102(2):169–176. doi: 10.1002/bjs.9725.

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