BACKGROUND: One of the prerequisites for proper healing of the anastomosis after a colorectal resection is adequate blood supply to the connected intestinal segments. It has been proposed that adequate visualization of the blood flow using indocyanine green (ICG) could lead to the reduction in the incidence of anastomotic leakage (AL). The aim of this study was to assess the effectiveness of intraoperative fluorescence angiography (FA) in decreasing the incidence of AL after minimally invasive low anterior resection (LAR) with total mesorectal excision (TME) in rectal cancer patients and to determine predictors of anastomotic leak. METHODS: From August 2015 to January 2019, data from 100 patients who underwent mini-invasive TME for rectal cancer using FA with indocyanine green (ICG) were prospectively collected and analyzed. They were compared with retrospectively analyzed data from a historical control group operated by one team of surgeons before the introduction of FA from November 2012 to August 2015 (100 patients). All patients from both groups were operated sequentially in one oncological center in Nový Jičín. RESULTS: The incidence of AL was significantly lower in the ICG group (19% vs. 9%, p = 0.042, χ2 test). In fifteen patients in the ICG group (15%), the resection line was moved due to insufficient perfusion. Using Pearson's χ2 test, diabetes (p = 0.036) and application of a transanal drain (NoCoil) (p = 0.032) were identified as other risk factors (RFs) for AL. CONCLUSION: The use of ICG to visualize tissue perfusion in low rectal resections for cancer can lead to a reduction of AL.

AGEL Research and Training Institute Prostejov Czech Republic

Department of Applied Mathematics Faculty of Electrical Engineering and Computer Science VSB Technical University of Ostrava Ostrava Czech Republic

Department of Surgery Faculty of Medicine and Dentistry Palacky University Olomouc Olomouc Czech Republic

Department of Surgery Faculty of Medicine University of Ostrava Ostrava Czech Republic

Department of Surgery Hospital Novy Jicin Purkyňova 2138 16 Novy Jicin 74101 Czech Republic

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Platell C, Barwood N, Dorfmann G et al (2007) The incidence of anastomotic leaks in patients undergoing colorectal surgery. Colorectal Dis 9:71–79. https://doi.org/10.1111/j.1463-1318.2006.01002.x PubMed DOI

van Geldere D, Fa-Si-Oen P, Noach LA et al (2002) Complications after colorectal surgery without mechanical bowel preparation. J Am Coll Surg 194:40–47. https://doi.org/10.1016/S1072-7515(01)01131-0 PubMed DOI

Boccola MA, Lin J, Rozen WM et al (2010) Reducing anastomotic leakage in oncologic colorectal surgery: an evidence-based review. Anticancer Res 30:601–607 PubMed

Hyman N, Manchester TL, Osler T et al (2007) Anastomotic leaks after intestinal anastomosis: it’s later than you think. Ann Surg 245:254–258. https://doi.org/10.1097/01.sla.0000225083.27182.85 PubMed DOI PMC

Reinke CE, Showalter S, Mahmoud NN et al (2013) Comparison of anastomotic leak rate after colorectal surgery using different databases. Dis Colon Rectum 56:638–644. https://doi.org/10.1097/DCR.0b013e31827886db PubMed DOI

Buchs NC, Gervaz P, Secic M et al (2008) Incidence, consequences, and risk factors for anastomotic dehiscence after colorectal surgery: a prospective monocentric study. Int J Colorectal Dis 23:265–270. https://doi.org/10.1007/s00384-007-0399-3 PubMed DOI

Damen N, Spilsbury K, Levitt M et al (2017) Anastomotic leaks in colorectal surgery. ANZ J Surg 84:763–768. https://doi.org/10.1111/ans.12494 DOI

McDermott FD, Heeney A, Kelly ME et al (2015) Systematic review of preoperative, intraoperative and postoperative risk factors for colorectal anastomotic leaks. Br J Surg 102:462–479. https://doi.org/10.1002/bjs.9697 PubMed DOI

Nasirkhan MU, Abir F, Longo W et al (2006) Anastomotic disruption after large bowel resection. World J Gastroenterol 12:2497–2504. https://doi.org/10.3748/wjg.v12.i16.2497 PubMed DOI PMC

Boccola MA, Buettner PG, Rozen WM et al (2011) Risk factors and outcomes for anastomotic leakage in colorectal surgery: a single-institution analysis of 1576 patients. World J Surg 35:186–195. https://doi.org/10.1007/s00268-010-0831-7 PubMed DOI

Paun BC, Cassie S, MacLean AR et al (2010) Postoperative complications following surgery for rectal cancer. Ann Surg 251:807–818. https://doi.org/10.1097/SLA.0b013e3181dae4ed PubMed DOI

Eriksen MT, Wibe A, Norstein J et al (2005) Norwegian Rectal Cancer Group. Anastomotic leakage following routine mesorectal excision for rectal cancer in a national cohort of patients. Colorectal Dis 7:51–57. https://doi.org/10.1111/j.1463-1318.2004.00700.x PubMed DOI

Matthiessen P, Hallböök O, Rutegard J et al (2007) Defunctioning stoma reduces symptomatic anastomotic leakage after low anterior resection of the rectum for cancer: a randomized multicenter trial. Ann Surg 246:207–214. https://doi.org/10.1097/SLA.0b013e3180603024 PubMed DOI PMC

Bertelsen CA, Andreasen AH, Jorgensen T et al (2010) Anastomotic leakage after anterior resection for rectal cancer: short- and long-term outcome. Colorectal Dis 12:76–81. https://doi.org/10.1111/j.1463-1318.2009.01935.x DOI

Kang CY, Halabi WJ, Chaudhry OO et al (2013) Risk factors for anastomotic leakage after anterior resection for rectal cancer. JAMA Surg 148:65–71. https://doi.org/10.1001/2013.jamasurg.2 PubMed DOI

Caulfeld H, Hyman NH (2013) Anastomotic leak after low anterior resection: a spectrum of clinical entities. JAMA Surg 148:177–182. https://doi.org/10.1001/jamasurgery.2013.413 DOI

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. https://doi.org/10.1007/s10151-017-1731-8 PubMed DOI

Kracht M, Hay JM, Fagniez PL et al (1993) Ileocolonic anastomosis after right hemicolectomy for carcinoma: stapled or hand-sewn? A prospective, multicenter, randomized trial. Int J Colorectal Dis 8:29–33. https://doi.org/10.1007/bf00341273 PubMed DOI

Karliczek A, Harlaar NJ, Zeebregts CJ et al (2009) Surgeons lack predictive accuracy for anastomotic leakage in gastrointestinal surgery. Int J Colorectal Dis 4:569–576. https://doi.org/10.1007/s00384-009-0658-6 DOI

Roesel C, Schachtrupp A et al (2010) Intraoperative laser fluorescence angiography in colorectal surgery: a noninvasive analysis to reduce the rate of anastomotic leakage. Langenbeck’s Arch Surg 395:1025–1030. https://doi.org/10.1007/s00423-010-0699-x DOI

Jafari MD, Lee KH, Halabi WJ et al (2013) The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc 27:3003–3008. https://doi.org/10.1007/s00464-013-2832-8 PubMed DOI

Vignali A, Gianotti L, Braga M et al (2000) Altered microperfusion at the rectal stump is predictive for rectal anastomotic leak. Dis Colon Rectum 43:76–82. https://doi.org/10.1007/bf02237248 PubMed DOI

Darwich I, Rustanto D, Friedberg R, Willeke F (2019) Spectrophotometric assessment of bowel perfusion during low anterior resection: a prospective study. Updates Surg 71(4):677–686. https://doi.org/10.1007/s13304-019-00682-9 PubMed DOI PMC

Boni L, Fingerhut A (2017) Indocyanine green fluorescence angiography during laparoscopic low anterior resection: results of a case-matched study. Surg Endosc 31:1836–1840. https://doi.org/10.1007/s00464-016-5181-6 PubMed DOI

Skrovina M, Bencurik V, Martinek L et al (2019) The significance of intraoperative fluorescence angiography in miniinvasive low rectal resections. Videosurg Other Miniinvasive Tech. https://doi.org/10.5114/wiitm.2019.84851 PubMed DOI PMC

Kawada K, Hasegawa S, Wada T et al (2017) Evaluation of intestinal perfusion by ICG fluorescence imaging in laparoscopic colorectal surgery with DST anastomosis. Surg Endosc 31(3):1061–1069. https://doi.org/10.1007/s00464-016-5064-x PubMed DOI

Jafari MD, Lee KH, Halabi WJ et al (2013) The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc 27(8):3003–3008. https://doi.org/10.1007/s00464-013-2832-8 PubMed DOI

Watanabe J, Ishibe A, Suwa Y et al (2019) Indocyanine green fluorescence imaging to reduce the risk of anastomotic leakage in laparoscopic low anterior resection for rectal cancer: a propensity score-matched cohort study. Surg Endosc Mar. https://doi.org/10.1007/s00464-019-06751-9 DOI

Boni L, David G, Dionigi G et al (2016) Indocyanine green-enhanced fluorescence to assess bowel perfusion during laparoscopic colorectal resection. Surg Endosc 30:2736–2742. https://doi.org/10.1007/s00464-015-4540-z PubMed DOI

Rahbari NN, Weitz J, Hohenberger W et al (2010) Definition and grading of anastomotic leakage following anterior resection of the rectum: a proposal by the International Study Group of Rectal Cancer. Surgery 147:339–351. https://doi.org/10.1016/j.surg.2009.10.012 PubMed DOI

R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

Jafari MD, Wexner SD, Martz JE et al (2015) Perfusion assessment in laparoscopic left-sided/anterior resection (PILLAR II): a multi-institutional study. J Am Coll Surg 220:82–92. https://doi.org/10.1016/j.jamcollsurg.2014.09.015 PubMed DOI

Kingham TP, Pachter HL (2009) Colonic anastomotic leak: risk factors, diagnosis, and treatment. J Am Coll Surg 208:269–278. https://doi.org/10.1016/j.jamcollsurg.2008.10.015 PubMed DOI

Boyle NH, Manifold D, Jordan MH et al (2000) Intraoperative assessment of colonic perfusion using scanning laser Doppler flowmetry during colonic resection. J Am Coll Surg 191:504–510. https://doi.org/10.1016/s1072-7515(00)00709-2 PubMed DOI

Sheridan WG, Lowndes RH, Young HL (1987) Tissue oxygen tension as a predictor of colonic anastomotic healing. Dis Colon Rectum 30:867–871. https://doi.org/10.1007/bf02555426 PubMed DOI

Kologlu M, Yorganci K, Renda N et al (2000) Effect of local and remote ischemia-reperfusion injury on healing of colonic anastomoses. Surgery 128:99–104. https://doi.org/10.1067/msy.2000.107414 PubMed DOI

Mizrahi I, Wexner SD (2017) Clinical role of fluorescence imaging in colorectal surgery—a review. Expert Rev Med Dev 14:75–82. https://doi.org/10.1080/17434440.2017.1265444 DOI

Kudszus S, Roesel C, Schachtrupp A, Höer JJ (2010) Intraoperative laser fluorescence angiography in colorectal surgery: a non-invasive analysis to reduce the rate of anastomotic leakage. Langenbeck’s Arch Surg 395(8):1025–1030 DOI

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. https://doi.org/10.1111/j.1463-1318.2012.03101.x PubMed DOI

De Nardi P, Elmore U, Maggi G et al (2020) Intraoperative angiography with indocyanine green to assess anastomosis perfusion in patients undergoing laparoscopic colorectal resection: results of a multicenter randomized controlled trial. Surg Endosc 34:53. https://doi.org/10.1007/s00464-019-06730-0 PubMed DOI

Ris F, Hompes R, Cunningham C et al (2014) Near-infrared (NIR) perfusion angiography in minimally invasive colorectal surgery. Surg Endosc 28:2221–2226. https://doi.org/10.1007/s00464-014-3432-y PubMed DOI PMC

Boni L, David G, Mangano A et al (2015) Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc 29:2046–2055. https://doi.org/10.1007/s00464-014-3895-x PubMed DOI

Gröne J, Koch D, Kreis ME et al (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. https://doi.org/10.1111/codi.13031 PubMed DOI

Hellan M, Spinoglio G, Pigazzi A et al (2014) The influence of fluorescence imaging on the location of bowel transection during robotic left-sided colorectal surgery. Surg Endosc 28:1695–1702. https://doi.org/10.1007/s00464-013-3377-6 PubMed DOI

Alander JT, Kaartinen I, Laakso A et al (2012) A review of indocyanine green fluorescent imaging in surgery. Int J Biomed Imaging 2012:940–985. https://doi.org/10.1155/2012/940585 DOI

Cahill RA, Mortensen NJ (2010) Intraoperative augmented reality for laparoscopic colorectal surgery by intraoperative near infrared fluorescence imaging and optical coherence tomography. Minerva Chir 65:451–462 PubMed

Benya R, Quintana J, Brundage B (1989) Adverse reactions to indocyanine green: a case report and a review of the literature. Cathet Cardiovasc Diagn 17:231–233. https://doi.org/10.1002/ccd.1810170410 PubMed DOI

Ris F, Hompes R, Lindsey I, Cunningham C, Mortensen NJ, Cahill RA (2014) Near infra-red laparoscopic assessment of the adequacy of blood perfusion of intestinal anastomosis—a video vignette. Colorectal Dis 16(8):646–647. https://doi.org/10.1111/codi.12593 PubMed DOI

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(12):883–884. https://doi.org/10.1007/s10151-016-1547-y PubMed DOI

Keller DS, Joshi HM, Rodriguez-Justo M, Walsh D, Coffey JC, Chand M (2017) Using fluorescence lymphangiography to define the ileocolic mesentery: proof of concept for the watershed area using real-time imaging. Tech Coloproctol 21(9):757–760. https://doi.org/10.1007/s10151-017-1677-x PubMed DOI

Martínek L, Pazdírek F, Hoch J (2018) Intraoperative fluorescence angiography of colorectal anastomotic perfusion: a technical aspect. Rozhl Chir Spring 97(4):167–171

Chang YK et al (2018) The impact of indocyanine-green fluorescence angiogram on colorectal resection. The Surgeon. https://doi.org/10.1016/j.surge.2018.08.006 PubMed DOI

Son G, Kwon M, Kim Y et al (2018) Quantitative analysis of colon perfusion pattern using indocyanine green (ICG) angiography in laparoscopic colorectal surgery. Surg Endosc Sept. https://doi.org/10.1007/s00464-018-6439-y DOI

Diana M, Halvax P et al (2014) Real-time navigation by fluorescence-based enhanced reality for precise estimation of future anastomotic site in digestive surgery. Surg Endosc 28(11):3108–3118. https://doi.org/10.1007/s00464-014-3592-9 PubMed DOI

Vignali A, Fazio VW, Lavery IC et al (1997) Factors associated with the occurrence of leaks in stapled rectal anastomoses: a review of 1014 patients. J Am Coll Surg 85:105–113. https://doi.org/10.1016/s1072-7515(97)00018-5 DOI

Wang S, Zhang Z, Liu M (2016) Efficacy of transanal tube placement after anterior resection for rectal cancer: a systematic review and meta-analysis. World J Surg Oncol 14:92. https://doi.org/10.1186/s12957-016-0854-0 PubMed DOI PMC