Abstract
Background
In the present study, patients with colorectal anastomoses that were assessed with indocyanine green (ICG) fluorescence angiography (FA) were compared to patients who had only white light visual inspection of their anastomosis. The impact of change in surgical plan guided by ICG-FA on anastomotic leak (AL) rates was assessed.
Methods
PubMed, Scopus, Web of Science, and Cochrane Central Register of Controlled Trials were queried for eligible studies. Studies included were comparative cohort studies and randomized trials that compared perfusion assessment of colorectal anastomosis with ICG-FA and inspection under white light. Main outcome measures were change in surgical plan guided by ICG-FA and rates of AL. Risk of bias was assessed using RoB-2 and ROBINS-1 tools. Differences between the two groups in categorical and continuous variables were expressed as odds ratio (OR) with 95% confidence interval (CI) and weighted mean difference.
Results
This systematic review included 27 studies comprising 8786 patients (48.5% males). Using ICG-FA was associated with significantly lower odds of AL (OR 0.452; 95% CI 0.366–0.558) and complications (OR 0.747; 95% CI 0.592–0.943) than the control group. The weighted mean rate of change in surgical plan based on ICG-FA was 9.6% (95% CI 7.3–11.8) and varied from 0.64% to 28.75%. A change in surgical plan was associated with significantly higher odds of AL (OR 2.73; 95% CI 1.54–4.82).
Limitations
Technical heterogeneity due to using different dosage of ICG and statistical heterogeneity in operative time and complication rates.
Conclusion
Assessment of colorectal anastomoses with ICG-FA is likely to be associated with lower odds of anastomotic leak than is traditional white light assessment. Change in plan based on ICG-FA may be associated with higher odds of AL.
PROSPERO registration number: CRD42021235644.
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References
Davis B, Rivadeneira DE (2013) Complications of colorectal anastomoses: leaks, strictures, and bleeding. Surg Clin N Am 93(1):61–87. https://doi.org/10.1016/j.suc.2012.09.014
Thomas MS, Margolin DA (2016) Management of colorectal anastomotic leak. Clin Colon Rectal Surg 29(2):138–144. https://doi.org/10.1055/s-0036-1580630
Kim IY, Kim BR, Kim YW (2015) The impact of anastomotic leakage on oncologic outcomes and the receipt and timing of adjuvant chemotherapy after colorectal cancer surgery. Int J Surg 22:3–9. https://doi.org/10.1016/j.ijsu.2015.08.017
Wu Z, van de Haar RC, Sparreboom CL et al (2016) Is the intraoperative air leak test effective in the prevention of colorectal anastomotic leakage? A systematic review and meta-analysis. Int J Colorectal Dis 31(8):1409–1417. https://doi.org/10.1007/s00384-016-2616-4
Li VK, Wexner SD, Pulido N, Wang H, Jin HY, Weiss EG, Nogeuras JJ, Sands DR (2009) Use of routine intraoperative endoscopy in elective laparoscopic colorectal surgery: can it further avoid anastomotic failure? Surg Endosc 23(11):2459–2465. https://doi.org/10.1007/s00464-009-0416-4
Emile SH, Gilshtein H, Wexner SD (2020) Quadruple assessment of colorectal anastomoses: a technique to reduce the incidence of anastomotic leakage. Colorectal Dis 22(1):102–103. https://doi.org/10.1111/codi.14844
Pommergaard HC, Achiam MP, Burcharth J, Rosenberg J (2015) Impaired blood supply in the colonic anastomosis in mice compromises healing. Int Surg 100(1):70–76. https://doi.org/10.9738/INTSURG-D-13-00191.1
Sujatha-Bhaskar S, Jafari MD, Stamos MJ (2017) The role of fluorescent angiography in anastomotic leaks. Surg Technol Int 25(30):83–88
Chan DKH, Lee SKF, Ang JJ (2020) Indocyanine green fluorescence angiography decreases the risk of colorectal anastomotic leakage: systematic review and meta-analysis. Surgery 168(6):1128–1137. https://doi.org/10.1016/j.surg.2020.08.024
Mok HT, Ong ZH, Yaow CYL, Ng CH, Buan BJL, Wong NW, Chong CS (2020) Indocyanine green fluorescent imaging on anastomotic leakage in colectomies: a network meta-analysis and systematic review. Int J Colorectal Dis 35(12):2365–2369. https://doi.org/10.1007/s00384-020-03723-7
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71. https://doi.org/10.1136/bmj.n71
Sterne JAC, Savović J, Page MJ, Elbers RG, Blencowe NS, Boutron I et al (2019) RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ 366:l4898
Sterne JAC, Hernán MA, Reeves BC, Savović J, Berkman ND, Viswanathan M et al (2016) ROBINS-I: a tool for assessing risk of bias in non-randomized studies of interventions. BMJ 355:i4919. https://doi.org/10.1136/bmj.i4919
Balshem H, Helfand M, Schunemann HJ, Oxman AD, Kunz R, Brozek J et al (2011) GRADE guidelines: 3. Rating the quality of evidence. J Clin Epidemiol 64(4):401–406
Yanagita T, Hara M, Osaga S, Nakai N, Maeda Y, Shiga K, Hirokawa T, Matsuo Y, Takahashi H, Takiguchi S (2021) 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. https://doi.org/10.1007/s00464-020-08230-y
Marquardt C, Kalev G, Schiedeck T (2020) Intraoperative fluorescence angiography with indocyanine green: retrospective evaluation and detailed analysis of our single-center 5-year experience focused on colorectal surgery. Innov Surg Sci 5(1–2):35–42. https://doi.org/10.1515/iss-2020-0009
Losurdo P, Mis TC, Cosola D, Bonadio L, Giudici F, Casagranda B, Bortul M, de Manzini N (2020) Anastomosis leak: is there still a place for indocyanine green fluorescence imaging in colon-rectal surgery? A Retrospective propensity score-matched cohort study. Surg Innov 25:1553350620975258. https://doi.org/10.1177/1553350620975258
Benčurik V, Škrovina M, Martínek L, Bartoš J, Macháčková M, Dosoudil M, Štěpánová E, Přibylová L, Briš R, Vomáčková K (2020) Intraoperative fluorescence angiography and risk factors of anastomotic leakage in mini-invasive low rectal resections. Surg Endosc. https://doi.org/10.1007/s00464-020-07982-x
Su H, Wu H, Bao M, Luo S, Wang X, Zhao C, Liu Q, Wang X, Zhou Z, Zhou H (2020) Indocyanine green fluorescence imaging to assess bowel perfusion during totally laparoscopic surgery for colon cancer. BMC Surg 20(1):102. https://doi.org/10.1186/s12893-020-00745-4
Alekseev M, Rybakov E, Shelygin Y, Chernyshov S, Zarodnyuk I (2020) A study investigating the perfusion of colorectal anastomoses using fluorescence angiography: results of the FLAG randomized trial. Colorectal Dis. https://doi.org/10.1111/codi.15037
Bonadio L, Iacuzzo C, Cosola D, Cipolat Mis T, Giudici F, Casagranda B et al (2020) Indocyanine green-enhanced fluorangiography (ICGf) in laparoscopic extraperitoneal rectal cancer resection. Updates Surg 72(2):477–482
De Nardi P, Elmore U, Maggi G, Maggiore R, Boni L, Cassinotti E 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(1):53–60
Hasegawa H, Tsukada Y, Wakabayashi M, Nomura S, Sasaki T, Nishizawa Y et al (2020) Impact of intraoperative indocyanine green fluorescence angiography on anastomotic leakage after laparoscopic sphincter-sparing surgery for malignant rectal tumors. Int J Colorectal Dis 35(3):471–480
Impellizzeri HG, Pulvirenti A, Inama M, Bacchion M, Marrano E, Creciun M et al (2020) Near-infrared fluorescence angiography for colorectal surgery is associated with a reduction of anastomotic leak rate. Updates Surg 72(4):991–998
Ishii M, Hamabe A, Okita K, Nishidate T, Okuya K, Usui A et al (2020) Efficacy of indocyanine green fluorescence angiography in preventing anastomotic leakage after laparoscopic colorectal cancer surgery. Int J Colorectal Dis 35(2):269–275
Watanabe J, Ishibe A, Suwa Y, Suwa H, Ota M, Kunisaki C et al (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(1):202–208
Tsang YP, Leung LA, Lau CW, Tang CN (2020) Indocyanine green fluorescence angiography to evaluate anastomotic perfusion in colorectal surgery. Int J Colorectal Dis 35(6):1133–1139
Wojcik M, Doussot A, Manfredelli S, Duclos C, Paquette B, Turco C et al (2020) Intra-operative fluorescence angiography is reproducible and reduces the rate of anastomotic leak after colorectal resection for cancer: a prospective case-matched study. Colorectal Dis 22(10):1263–1270
Skrovina M, Bencurik V, Martinek L, Machackova M, Bartos J, Andel P et al (2020) The significance of intraoperative fluorescence angiography in miniinvasive low rectal resections. Wideochir Inne Tech Maloinwazyjne 15(1):43–48
Otero-Piñeiro AM, de Lacy FB, Van Laarhoven JJ, Martín-Perez B, Valverde S, Bravo R et al (2020) The impact of fluorescence angiography on anastomotic leak rate following transanal total mesorectal excision for rectal cancer: a comparative study. Surg Endosc 35:754–762
Spinelli A, Carvello M, Kotze PG, Maroli A, Montroni I, Montorsi M et al (2019) Ileal pouch-anal anastomosis with fluorescence angiography: a case-matched study. Colorectal Dis 21(7):827–832
Dinallo AM, Kolarsick P, Boyan WP, Protyniak B, James A, Dressner RM et al (2019) Does routine use of indocyanine green fluorescence angiography prevent anastomotic leaks? A retrospective cohort analysis. Am J Surg 218(1):136–139
Shapera E, Hsiung RW (2019) Assessment of anastomotic perfusion in left-sided robotic assisted colorectal resection by indocyanine green fluorescence angiography. Minim Invasive Surg 2019:3267217
Wada T, Kawada K, Hoshino N, Inamoto S, Yoshitomi M, Hida K et al (2019) The effects of intraoperative ICG fluorescence angiography in laparoscopic low anterior resection: a propensity score-matched study. Int J Clin Oncol 24(4):394–402
Ris F, Liot E, Buchs NC, Kraus R, Ismael G, Belfontali V et al (2018) Near-infrared anastomotic perfusion assessment network VOIR. Multicentre phase II trial of near-infrared imaging in elective colorectal surgery. Br J Surg 105(10):1359–1367
Mizrahi I, Abu-Gazala M, Rickles AS, Fernandez LM, Petrucci A, Wolf J et al (2018) Indocyanine green fluorescence angiography during low anterior resection for low rectal cancer: results of a comparative cohort study. Tech Coloproctol 22:535–540. https://doi.org/10.1007/s10151-018-1832-z
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(4):1836–1840
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(4):376–384
Kin C, Vo H, Welton L, Welton M (2015) Equivocal effect of intraoperative fluorescence angiography on colorectal anastomotic leaks. Dis Colon Rectum 58(6):582–587. https://doi.org/10.1097/DCR.0000000000000320
Jafari MD, Lee KH, Halabi WJ, Mills SD, Carmichael JC, Stamos MJ 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
Kudszus S, Roesel C, Schachtrupp A, Höer JJ (2010) Intraoperative laser fluorescence angiography in colorectal surgery: a noninvasive analysis to reduce the rate of anastomotic leakage. Langenbecks Arch Surg 395:1025–1030
Telem DA, Chin EH, Nguyen SQ, Divino CM (2010) Risk factors for anastomotic leak following colorectal surgery: a case-control study. Arch Surg 145(4):371–376. https://doi.org/10.1001/archsurg.2010.40
Kryzauskas M, Poskus E, Dulskas A et al (2020) The problem of colorectal anastomosis safety. Medicine 99(2):e18560. https://doi.org/10.1097/MD.0000000000018560
Zhang C, Li A, Luo T, Li Y, Li F, Li J (2020) Evaluation of characteristics of left-sided colorectal perfusion in elderly patients by angiography. World J Gastroenterol 26(24):3484–3494. https://doi.org/10.3748/wjg.v26.i24.3484
Shalaby M, Thabet W, Morshed M, Farid M, Sileri P (2019) Preventive strategies for anastomotic leakage after colorectal resections: a review. World J Meta-Anal 7(8):389–398
Stephensen BD, Reid F, Shaikh S, Carroll R, Smith SR, Pockney P, PREDICT Study Group collaborators (2020) C-reactive protein trajectory to predict colorectal anastomotic leak: PREDICT study. Br J Surg 107(13):1832–1837. https://doi.org/10.1002/bjs.11812
Rawlinson A, Kang P, Evans J, Khanna A (2011) A systematic review of enhanced recovery protocols in colorectal surgery. Ann R Coll Surg Engl 93(8):583–588. https://doi.org/10.1308/147870811X605219
Hajjar R, Santos MM, Dagbert F, Richard CS (2019) Current evidence on the relation between gut microbiota and intestinal anastomotic leak in colorectal surgery. Am J Surg 218(5):1000–1007. https://doi.org/10.1016/j.amjsurg.2019.07.001
Diana M (2017) Enabling precision digestive surgery with fluorescence imaging. Transl Gastroenterol Hepatol 21(2):97. https://doi.org/10.21037/tgh.2017.11.06
Diana M, Noll E, Diemunsch P et al (2014) Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg 259:700–707. https://doi.org/10.1097/SLA.0b013e31828d4ab3
Armstrong G, Croft J, Corrigan N, Brown JM, Goh V, Quirke P et al (2018) IntAct: intra-operative fluorescence angiography to prevent anastomotic leak in rectal cancer surgery: a randomized controlled trial. Colorectal Dis 20(8):O226–O234. https://doi.org/10.1111/codi.14257
Funding
Steven D. Wexner is a paid consultant for Stryker, Intuitive Surgical, Olympus, and Medtronic and receives royalty payments from Karl Storz Endoscopy America, Medtronic, and Intuitive Surgical.
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SE designed the study, collected the data, assessed the quality of the studies, conducted data analysis, and wrote the manuscript. SK contributed to data collection and interpretation, quality assessment of studies, and revision of the manuscript. SW contributed to data interpretation and critically revised the manuscript.
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Sameh Emile and Sualeh Khan have no conflict of interests or financial ties to disclose.
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Supplementary file2 Supp Figure 1. Funnel plot for assessment of publication bias in outcome “impact of change in surgical plan on leak rate” (PNG 7 kb)
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Supplementary file3 Supp Figure 2. Funnel plot for assessment of publication bias in outcome “Rate of anastomotic leak in ICG versus control group” (JPG 27 kb)
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Supplementary file4 Supp Figure 3. Funnel plot for assessment of publication bias in outcome “Rate of Ileus in ICG versus control group” (PNG 7 kb)
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Supplementary file5 Supp Figure 4. Funnel plot for assessment of publication bias in outcome “Rate of complications in ICG versus control group” (PNG 7 kb)
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Supplementary file6 Supp Figure 5. Funnel plot for assessment of publication bias in outcome “operation time in ICG versus control group” (PNG 6 kb)
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Emile, S.H., Khan, S.M. & Wexner, S.D. Impact of change in the surgical plan based on indocyanine green fluorescence angiography on the rates of colorectal anastomotic leak: a systematic review and meta-analysis. Surg Endosc 36, 2245–2257 (2022). https://doi.org/10.1007/s00464-021-08973-2
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DOI: https://doi.org/10.1007/s00464-021-08973-2