Abstract
Background
Intestinal perfusion at the anastomotic site is thought to be one of the most influential risk factors for postoperative anastomotic leakage (AL). We evaluated the efficacy of indocyanine green (ICG) fluorescence imaging at the stump of the proximal colon in left-sided colectomy or rectal resection in terms of decreasing the incidence of AL.
Methods
Prospectively collected data were retrospectively evaluated. Patients who underwent left-sided colectomy or rectal resection were enrolled (ICG group; n = 197), and patients who had undergone a similar procedure before the ICG group were enrolled from the charts as historical controls (HC group; n = 187). After ICG evaluation, anastomosis was performed where fluorescence was sufficient. The incidence of AL was compared between the ICG and HC groups. Propensity score (PS)-matched data were analyzed to clarify the risk of AL.
Results
AL occurred in 6 patients (3.3%) in the ICG group and 17 (10.7%) in the HC group. ICG evaluation revealed 179 patients with good fluorescence and 18 with poor/none perfusion (9.1%). The transection line was changed in all patients with poor/none fluorescence. Three of these 18 patients developed AL (16.7%), though transection line was changed at which is thought to be good. We hope AL in poor/none fluorescence can be prevented at the same rate of cases with good fluorescence. Actually, the rate of that was significantly higher compared with good fluorescence patients (P = 0.038). 93 patients in each group were compared by PS-matched data analysis, which showed the AL rate in the ICG group was significantly lower than that in the HC group (3.2% vs 10.8%, respectively; P = 0.046).
Conclusions
Even though this study has limitations of comparison of data prospectively collected and retrospectively analyzed, intraoperative ICG fluorescence imaging evaluation could significantly decrease the incidence of AL.
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References
Ohigashi S, Taketa T, Shimada G, Kubota K, Sunagawa H, Kishida A (2018) Fruitful first experience with an 8K ultra-high-definition endoscope for laparoscopic colorectal surgery. Asian J Endosc Surg. https://doi.org/10.1111/ases.12638
Mirnezami A, Mirnezami R, Chandrakumaran K, Sasapu K, Sagar P, Finan P (2011) Increased local recurrence and reduced survival from colorectal cancer following anastomotic leak: systematic review and meta-analysis. Ann Surg 253:890–899
Kang J, Choi GS, Oh JH, Kim NK, Park JS, Kim MJ, Lee KY, Baik SH (2015) Multicenter analysis of long-term oncologic impact of anastomotic leakage after laparoscopic total mesorectal excision: the Korean Laparoscopic Colorectal Surgery Study Group. Medicine (Baltimore) 94:e1202
Ramphal W, Boeding JRE, Gobardhan PD, Rutten HJT, de Winter L, Crolla R, Schreinemakers JMJ (2018) Oncologic outcome and recurrence rate following anastomotic leakage after curative resection for colorectal cancer. Surg Oncol 27:730–736
Ha GW, Kim JH, Lee MR (2017) Oncologic impact of anastomotic leakage following colorectal cancer surgery: a systematic review and meta-analysis. Ann Surg Oncol 24:3289–3299
Kim CW, Baek SJ, Hur H, Min BS, Baik SH, Kim NK (2016) Anastomotic leakage after low anterior resection for rectal cancer is different between minimally invasive surgery and open surgery. Ann Surg 263:130–137
Qin Q, Ma T, Deng Y, Zheng J, Zhou Z, Wang H, Wang L, Wang J (2016) Impact of preoperative radiotherapy on anastomotic leakage and stenosis after rectal cancer resection: post hoc analysis of a randomized controlled trial. Dis Colon Rectum 59:934–942
Kawada K, Sakai Y (2016) Preoperative, intraoperative and postoperative risk factors for anastomotic leakage after laparoscopic low anterior resection with double stapling technique anastomosis. World J Gastroenterol 22:5718–5727
Jung SH, Yu CS, Choi PW, Kim DD, Park IJ, Kim HC, Kim JC (2008) Risk factors and oncologic impact of anastomotic leakage after rectal cancer surgery. Dis Colon Rectum 51:902–908
Parthasarathy M, Greensmith M, Bowers D, Groot-Wassink T (2017) Risk factors for anastomotic leakage after colorectal resection: a retrospective analysis of 17 518 patients. Colorectal Dis 19:288–298
Vignali A, Gianotti L, Braga M, Radaelli G, Malvezzi L, Di Carlo V (2000) Altered microperfusion at the rectal stump is predictive for rectal anastomotic leak. Dis Colon Rectum 43:76–82
Jafari MD, Lee KH, Halabi WJ, Mills SD, Carmichael JC, Stamos MJ, Pigazzi A (2013) The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc 27:3003–3008
Boni L, David G, Dionigi G, Rausei S, Cassinotti E, Fingerhut A (2015) Indocyanine green-enhanced fluorescence to assess bowel perfusion during laparoscopic colorectal resection. Surg Endosc. https://doi.org/10.1007/s00464-015-4540-z
Boni L, David G, Mangano A, Dionigi G, Rausei S, Spampatti S, Cassinotti E, Fingerhut A (2015) Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc 29:2046–2055
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
Tamura K, Hotta T, Yokoyama S, Matsuda K, Iwamoto H, Yamaue H (2018) Using indocyanine green fluorescent imaging to successfully resect metachronous regional lymph node recurrence of rectosigmoid cancer. Asian J Endosc Surg 11:47–49
Watanabe J, Ishibe A, Suwa Y, Suwa H, Ota M, Kunisaki C, Endo I (2020) 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 34:202–208
Villegas-Tovar E, Jimenez-Lillo J, Jimenez-Valerio V, Diaz-Giron-Gidi A, Faes-Petersen R, Otero-Pineiro A, De Lacy FB, Martinez-Portilla RJ, Lacy AM (2020) Performance of Indocyanine green for sentinel lymph node map** and lymph node metastasis in colorectal cancer: a diagnostic test accuracy meta-analysis. Surg Endosc 34:1035–1047
Degett TH, Andersen HS, Gogenur I (2016) Indocyanine green fluorescence angiography for intraoperative assessment of gastrointestinal anastomotic perfusion: a systematic review of clinical trials. Langenbecks Arch Surg 401:767–775
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
Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213
Rahbari NN, Weitz J, Hohenberger W, Heald RJ, Moran B, Ulrich A, Holm T, Wong WD, Tiret E, Moriya Y, Laurberg S, den Dulk M, van de Velde C, Buchler MW (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
Ris F, Hompes R, Cunningham C, Lindsey I, Guy R, Jones O, George B, Cahill RA, Mortensen NJ (2014) Near-infrared (NIR) perfusion angiography in minimally invasive colorectal surgery. Surg Endosc 28:2221–2226
Fengler J (2015) Near-infrared fluorescence laparoscopy–technical description of PINPOINT(R) a novel and commercially available system. Colorectal Dis 17(Suppl 3):3–6
Nishigori N, Koyama F, Nakagawa T, Nakamura S, Ueda T, Inoue T, Kawasaki K, Obara S, Nakamoto T, Fujii H, Nakajima Y (2016) Visualization of lymph/blood flow in laparoscopic colorectal cancer surgery by ICG fluorescence imaging (Lap-IGFI). Ann Surg Oncol 23(Suppl 2):S266-274
Kawada K, Hasegawa S, Wada T, Takahashi R, Hisamori S, Hida K, Sakai Y (2017) Evaluation of intestinal perfusion by ICG fluorescence imaging in laparoscopic colorectal surgery with DST anastomosis. Surg Endosc 31:1061–1069
Spinelli A, Cantore F, Kotze PG, David G, Sacchi M, Carvello M (2017) Fluorescence angiography during transanal trans-stomal proctectomy and ileal pouch anal anastomosis: a video vignette. Colorectal Dis. https://doi.org/10.1111/codi.13992
Kin C, Vo H, Welton L, Welton M (2015) Equivocal effect of intraoperative fluorescence angiography on colorectal anastomotic leaks. Dis Colon Rectum 58:582–587
Kim JC, Lee JL, Park SH (2017) Interpretative guidelines and possible indications for indocyanine green fluorescence imaging in robot-assisted sphincter-saving operations. Dis Colon Rectum 60:376–384
Shen R, Zhang Y, Wang T (2018) Indocyanine green fluorescence angiography and the incidence of anastomotic leak after colorectal resection for colorectal cancer: a meta-analysis. Dis Colon Rectum 61:1228–1234
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
Chang YK, Foo CC, Yip J, Wei R, Ng KK, Lo O, Choi HK, Law WL (2018) The impact of indocyanine-green fluorescence angiogram on colorectal resection. Surgeon. https://doi.org/10.1016/j.surge.2018.08.006
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 (2018) Multicentre phase II trial of near-infrared imaging in elective colorectal surgery. Br J Surg 105:1359–1367
van den Bos J, Jongen A, Melenhorst J, Breukink SO, Lenaerts K, Schols RM, Bouvy ND, Stassen LPS (2019) Near-infrared fluorescence image-guidance in anastomotic colorectal cancer surgery and its relation to serum markers of anastomotic leakage: a clinical pilot study. Surg Endosc. https://doi.org/10.1007/s00464-019-06673-6
Wada T, Kawada K, Takahashi R, Yoshitomi M, Hida K, Hasegawa S, Sakai Y (2017) ICG fluorescence imaging for quantitative evaluation of colonic perfusion in laparoscopic colorectal surgery. Surg Endosc 31:4184–4193
Son GM, Kwon MS, Kim Y, Kim J, Kim SH, Lee JW (2018) Quantitative analysis of colon perfusion pattern using indocyanine green (ICG) angiography in laparoscopic colorectal surgery. Surg Endosc. https://doi.org/10.1007/s00464-018-6439-y
Acknowledgements
This research was supported by the surgical team in our hospital. We thank our colleagues who provided insight and expertise that greatly assisted the research. We would like to thank Ms. Nobuko Yamada, a secretary in our surgical department, who greatly assisted in the registration of this research, and appreciate voluntary help of Dr. Tamaki Layman and Dr. Ronald Layman.
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Drs. Takeshi Yanagita, Masayasu Hara, Satoshi Osaga, Nozomu Nakai, Yuzo Maeda, Kazuyoshi Shiga, Takahisa Hirokawa, Yoichi Matsuo, Hiroki Takahashi, and Shuji Takiguchi have no conflicts of interest or financial ties to disclose.
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Yanagita, T., Hara, M., Osaga, S. et al. Efficacy of intraoperative ICG fluorescence imaging evaluation for preventing anastomotic leakage after left-sided colon or rectal cancer surgery: a propensity score-matched analysis. Surg Endosc 35, 2373–2385 (2021). https://doi.org/10.1007/s00464-020-08230-y
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DOI: https://doi.org/10.1007/s00464-020-08230-y