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Effect of indocyanine green fluorescence angiography on preventing anastomotic leakage after colorectal surgery: a meta-analysis

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Abstract

Anastomotic leakage (AL) is a serious but not uncommon complication after colorectal surgery. We conducted this study to evaluate the effect of routine indocyanine green fluorescence angiography (ICG-FA) on reducing the AL rate after colorectal surgery. We identified all research articles about colorectal surgery using ICG-FA, published in the PubMed, EMBASE, and Cochrane Library databases from the date of database establishment to May 2020. Revman 5.3 was used for statistical analysis. We analyzed 22 controlled studies and 7 non-controlled studies on ICG-FA, including 6312 patients. The controlled studies included 2354 patients in the ICG group and 3522 patients in the non-ICG group. Meta-analysis showed that ICG-FA reduced the AL rate after colorectal surgery significantly (RR = 0.39; 95% CI 0.30–0.50; P < 0.00001). However, patients whose resection line was changed based on the fluorescence angiography had a higher AL rate than those whose resection line was not changed (OR = 5.37; 95% CI 2.67–10.81; P < 0.00001). The overall complication rate, severe complication rate, and reoperation rate in the ICG group were significantly lower than those in the non-ICG group (RR = 0.79, 95% CI 0.67–0.92, P = 0.002; RR = 0.67, 95% CI 0.47–0.96, P = 0.03; RR = 0.53, 95% CI 0.29–0.96, P = 0.04, respectively), whereas the postoperative ileus rate was significantly higher in the ICG group than in the non-ICG group (RR = 1.65; 95% CI 1.09–2.50; P = 0.02), especially in Western countries (RR = 1.6; 95% CI 1.04–2.47; P = 0.03).

ICG-FA may reduce the AL rate after colorectal surgery, but ICG-FA group patients with transection line change for insufficient blood perfusion to the anastomotic stoma after evaluation had a higher AL rate than those without transection line change. Therefore, ICG-FA can help to identify patients at high risk of AL and intercept its occurrence. Moreover, ICG-FA may reduce the overall complication rate, severe complication rate, and reoperation rate, but induce postoperative ileus. High-quality randomized-controlled trials with a placebo control are needed to further evaluate the effectiveness and safety of ICG-FA.

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Abbreviations

ICG:

Indocyanine green

FA:

Fluorescence angiography

NIR:

Near-infrared

AL:

Anastomotic leakage

RCTs:

Randomized-controlled trials

RCSs:

Retrospective cohort studies

PCSs:

Prospective cohort studies

References

  1. Landsman ML, Kwant G, Mook GA, Zijlstra WG. Light-absorbing properties, stability, and spectral stabilization of indocyanine green. J Appl Physiol. 1976;40(4):575–83.

    Article  CAS  Google Scholar 

  2. Guyer DR, Puliafito CA, Monés JM, Friedman E, Chang W, Verdooner SR. Digital indocyanine-green angiography in chorioretinal disorders. Ophthalmology. 1992;99(2):287–91.

    Article  CAS  Google Scholar 

  3. Nagata K, Endo S, Hidaka E, Tanaka J, Kudo SE, Shiokawa A. Laparoscopic sentinel node mapping for colorectal cancer using infrared ray laparoscopy. Anticancer Res. 2006;26(3B):2307–11.

    PubMed  Google Scholar 

  4. Rutegård M, Rutegård J. Anastomotic leakage in rectal cancer surgery: the role of blood perfusion. World J Gastrointest Surg. 2015;7(11):289–92.

    Article  Google Scholar 

  5. Blanco-Colino R, Espin-Basany E. Intraoperative use of ICG fluorescence imaging to reduce the risk of anastomotic leakage in colorectal surgery: a systematic review and meta-analysis. Tech Coloproctol. 2018;22(1):15–23.

    Article  CAS  Google Scholar 

  6. Shen R, Zhang Y, Wang T. Indocyanine green fluorescence angiography and the incidence of anastomotic leak after colorectal resection for colorectal cancer: a meta-analysis. Dis Colon Rectum. 2018;61(10):1228–34.

    Article  Google Scholar 

  7. Shen Y, Yang T, Yang J, Meng W, Wang Z. Intraoperative indocyanine green fluorescence angiography to prevent anastomotic leak after low anterior resection for rectal cancer: a meta-analysis. ANZ J Surg. 2020. https://doi.org/10.1111/ans.15809.

    Article  PubMed  Google Scholar 

  8. Alekseev M, Rybakov E, Shelygin Y, Chernyshov S, Zarodnyuk I. A study investigating the perfusion of colorectal anastomoses using fluorescence angiography: results of the FLAG randomized trial. Colorectal Dis. 2020. https://doi.org/10.1111/codi.15037.

    Article  PubMed  Google Scholar 

  9. Bonadio L, Iacuzzo C, Cosola D, Cipolat Mis T, Giudici F, Casagranda B, et al. Indocyanine green-enhanced fluorangiography (ICGf) in laparoscopic extraperitoneal rectal cancer resection. Updates Surg. 2020;72(2):477–82.

    Article  Google Scholar 

  10. De Nardi P, Elmore U, Maggi G, Maggiore R, Boni L, Cassinotti E, et al. Intraoperative angiography with indocyanine green to assess anastomosis perfusion in patients undergoing laparoscopic colorectal resection: results of a multicenter randomized controlled trial. Surg Endosc. 2020;34(1):53–60.

    Article  Google Scholar 

  11. Dinallo AM, Kolarsick P, Boyan WP, Protyniak B, James A, Dressner RM, et al. Does routine use of indocyanine green fluorescence angiography prevent anastomotic leaks? A retrospective cohort analysis. Am J Surg. 2019;218(1):136–9.

    Article  Google Scholar 

  12. Hasegawa H, Tsukada Y, Wakabayashi M, Nomura S, Sasaki T, Nishizawa Y, et al. Impact of intraoperative indocyanine green fluorescence angiography on anastomotic leakage after laparoscopic sphincter-sparing surgery for malignant rectal tumors. Int J Colorectal Dis. 2020;35(3):471–80.

    Article  Google Scholar 

  13. Impellizzeri HG, Pulvirenti A, Inama M, Bacchion M, Marrano E, Creciun M, et al. Near-infrared fluorescence angiography for colorectal surgery is associated with a reduction of anastomotic leak rate. Updates Surg. 2020;72(4):991–8.

    Article  Google Scholar 

  14. Ishii M, Hamabe A, Okita K, Nishidate T, Okuya K, Usui A, et al. Efficacy of indocyanine green fluorescence angiography in preventing anastomotic leakage after laparoscopic colorectal cancer surgery. Int J Colorectal Dis. 2020;35(2):269–75.

    Article  Google Scholar 

  15. Kojima S, Sakamoto T, Matsui Y, Nambu K, Masamune K. Clinical efficacy of bowel perfusion assessment during laparoscopic colorectal resection using laser speckle contrast imaging: a matched case-control study. Asian J Endosc Surg. 2019. https://doi.org/10.1111/ases.12759.

    Article  PubMed  Google Scholar 

  16. Mizrahi I, Abu-Gazala M, Rickles AS, Fernandez LM, Petrucci A, Wolf J, et al. Indocyanine green fluorescence angiography during low anterior resection for low rectal cancer: results of a comparative cohort study. Tech Coloproctol. 2018;22(7):535–40.

    Article  CAS  Google Scholar 

  17. Otero-Piñeiro AM, de Lacy FB, Van Laarhoven JJ, Martín-Perez B, Valverde S, Bravo R, et al. The impact of fluorescence angiography on anastomotic leak rate following transanal total mesorectal excision for rectal cancer: a comparative study. Surg Endosc. 2020.

  18. Shapera E, Hsiung RW. Assessment of anastomotic perfusion in left-sided robotic assisted colorectal resection by indocyanine green fluorescence angiography. Minim Invasive Surg. 2019;2019:3267217.

    PubMed  PubMed Central  Google Scholar 

  19. Skrovina M, Bencurik V, Martinek L, Machackova M, Bartos J, Andel P, et al. The significance of intraoperative fluorescence angiography in miniinvasive low rectal resections. Wideochir Inne Tech Maloinwazyjne. 2020;15(1):43–8.

    PubMed  Google Scholar 

  20. Spinelli A, Carvello M, Kotze PG, Maroli A, Montroni I, Montorsi M, et al. Ileal pouch-anal anastomosis with fluorescence angiography: a case-matched study. Colorectal Dis. 2019;21(7):827–32.

    CAS  PubMed  Google Scholar 

  21. Tsang YP, Leung LA, Lau CW, Tang CN. Indocyanine green fluorescence angiography to evaluate anastomotic perfusion in colorectal surgery. Int J Colorectal Dis. 2020;35(6):1133–9.

    Article  Google Scholar 

  22. Wojcik M, Doussot A, Manfredelli S, Duclos C, Paquette B, Turco C, et al. 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. 2020;22(10):1263–70.

    Article  CAS  Google Scholar 

  23. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol. 2009;62(10):e1-34.

    Article  Google Scholar 

  24. Boni L, Fingerhut A, Marzorati A, Rausei S, Dionigi G, Cassinotti E. Indocyanine green fluorescence angiography during laparoscopic low anterior resection: results of a case-matched study. Surg Endosc. 2017;31(4):1836–40.

    Article  Google Scholar 

  25. Jafari MD, Lee KH, Halabi WJ, Mills SD, Carmichael JC, Stamos MJ, et al. The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc. 2013;27(8):3003–8.

    Article  Google Scholar 

  26. Kim JC, Lee JL, Kim CW, Lim SB, Alsaleem HA, Park SH. Mechanotechnical faults and particular issues of anastomotic complications following robot-assisted anterior resection in 968 rectal cancer patients. J Surg Oncol. 2019;120(8):1436–45.

    Article  Google Scholar 

  27. Kim JC, Lee JL, Park SH. Interpretative guidelines and possible indications for indocyanine green fluorescence imaging in robot-assisted sphincter-saving operations. Dis Colon Rectum. 2017;60(4):376–84.

    Article  Google Scholar 

  28. 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):1025–30.

    Article  Google Scholar 

  29. Wada T, Kawada K, Hoshino N, Inamoto S, Yoshitomi M, Hida K, et al. The effects of intraoperative ICG fluorescence angiography in laparoscopic low anterior resection: a propensity score-matched study. Int J Clin Oncol. 2019;24(4):394–402.

    Article  Google Scholar 

  30. Watanabe J, Ishibe A, Suwa Y, Suwa H, Ota M, Kunisaki C, et al. 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. 2020;34(1):202–8.

    Article  Google Scholar 

  31. Ris F, Liot E, Buchs NC, Kraus R, Ismael G, Belfontali V, et al. Near-infrared anastomotic perfusion assessment network VOIR. Multicentre phase II trial of near-infrared imaging in elective colorectal surgery. Br J Surg. 2018;105(10):1359–67.

    Article  CAS  Google Scholar 

  32. Alexeev MV, Shelygin YA, Rybakov EG. Primenenie intraoperatsionnoĭ fliuorestsentnoĭ angiografii v kachestve metoda profilaktiki nesostoiatel'nosti kolorektal'nogo anastomoza: rezul'taty prospektivnogo issledovaniia [Prevention of colorectal anastomotic leakage by using of intraoperative fluorescent angiography: prospective trial data]. Khirurgiia (Mosk). 2018; (8. Vyp. 2):47–51. Russian.

  33. Gröne J, Koch D, Kreis ME. Impact of intraoperative microperfusion assessment with Pinpoint Perfusion Imaging on surgical management of laparoscopic low rectal and anorectal anastomoses. Colorectal Dis. 2015;17(Suppl 3):22–8.

    Article  Google Scholar 

  34. 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):1695–702.

    Article  Google Scholar 

  35. Kawada K, Hasegawa S, Wada T, Takahashi R, Hisamori S, Hida K, et al. Evaluation of intestinal perfusion by ICG fluorescence imaging in laparoscopic colorectal surgery with DST anastomosis. Surg Endosc. 2017;31(3):1061–9.

    Article  Google Scholar 

  36. Morales-Conde S, Alarcón I, Yang T, Licardie E, Camacho V, Del Aguilar F, et al. Fluorescence angiography with indocyanine green (ICG) to evaluate anastomosis in colorectal surgery: where does it have more value? Surg Endosc. 2019;34(9):3897–907.

    Article  Google Scholar 

  37. van den Bos J, Jongen ACHM, Melenhorst J, Breukink SO, Lenaerts K, Schols RM, et al. 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. 2019;33(11):3766–74.

    Article  Google Scholar 

  38. Wada T, Kawada K, Takahashi R, Yoshitomi M, Hida K, Hasegawa S, et al. ICG fluorescence imaging for quantitative evaluation of colonic perfusion in laparoscopic colorectal surgery. Surg Endosc. 2017;31(10):4184–93.

    Article  Google Scholar 

  39. McDermott FD, Heeney A, Kelly ME, Steele RJ, Carlson GL, Winter DC. Systematic review of preoperative, intraoperative and postoperative risk factors for colorectal anastomotic leaks. Br J Surg. 2015;102(5):462–79.

    Article  CAS  Google Scholar 

  40. Protyniak B, Dinallo AM, Boyan WP Jr, Dressner RM, Arvanitis ML. Intraoperative indocyanine green fluorescence angiography–an objective evaluation of anastomotic perfusion in colorectal surgery. Am Surg. 2015;81(6):580–4.

    Article  Google Scholar 

  41. Matsui A, Winer JH, Laurence RG, Frangioni JV. Predicting the survival of experimental ischaemic small bowel using intraoperative near-infrared fluorescence angiography. Br J Surg. 2011;98(12):1725–34.

    Article  CAS  Google Scholar 

  42. Diana M, Noll E, Diemunsch P, Dallemagne B, Benahmed MA, Agnus V, et al. Enhanced-reality video fluorescence: a real-time assessment of intestinal viability. Ann Surg. 2014;259(4):700–7.

    Article  Google Scholar 

  43. Son GM, Kwon MS, Kim Y, Kim J, Kim SH, Lee JW. Quantitative analysis of colon perfusion pattern using indocyanine green (ICG) angiography in laparoscopic colorectal surgery. Surg Endosc. 2019;33(5):1640–9.

    Article  Google Scholar 

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Acknowledgements

We thank all the reviewers and editors for their helpful suggestions to improve the quality of our paper. Everyone who contributed to the article met the criteria for authorship, including those who provided professional writing services or materials.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. We have no conflicts of interest to declare.

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WZ was responsible for drafting the manuscript, as well as the acquisition, analysis, and interpretation of data. XC contributed to the concept and design of the study. Both authors read and approved the final manuscript.

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Correspondence to Xu Che.

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Drs. Zhang Wei and Che Xu have no conflicts of interest or financial ties to disclose.

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Ethical approval was not necessary, as this study was a “Systematic Review and Meta-analysis.” There are no individual person's data or details of case reports disclosed in this article.

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Zhang, W., Che, X. Effect of indocyanine green fluorescence angiography on preventing anastomotic leakage after colorectal surgery: a meta-analysis. Surg Today 51, 1415–1428 (2021). https://doi.org/10.1007/s00595-020-02195-0

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