Abstract
The blood supply of the right gastroepiploic artery after esophagectomy with gastric tube reconstruction is essential for avoiding anastomotic leakage. Near-infrared fluorescence (NIRF) imaging with indocyanine green is widely used to assess the blood supply because it can visualize it in real-time during navigation surgery. However, there is no established protocol for this modality. One reason for this lack of protocol is that NIRF provides subjective information. This study aimed to evaluate NIRF quantification. We conducted a literature review of risk factors for anastomotic leakage after esophagectomy, NIRF procedures, NIRF quantification, and new methods to compensate for NIRF limitations. Major methods for the quantification of NIRF include measuring the blood flow speed, visualization time, and fluorescence intensity. The cutoff value for the blood flow speed is 2.07 cm/s, and that for the visualization time is 30–90 s. Although the time-intensity curve provided patterns of change in the blood flow, it did not show an association with anastomotic leakage. However, to compensate for the limitations of NIRF, new devices have been reported that can assess tissue oxygenation perfusion, organ hemoglobin concentration, and microcirculation.
References
Akiyama H, Miyazono H, Tsurumaru M, Hashimoto C, Kawamura T. Use of the stomach as an esophageal substitute. Ann Surg. 1978;188:606–10.
Takeuchi H, Miyata H, Gotoh M, Kitagawa Y, Baba H, Kimura W, et al. A risk model for esophagectomy using data of 5354 patients included in a Japanese nationwide web-based database. Ann Surg. 2014;260:259–66.
Biere SS, van Berge Henegouwen MI, Maas KW, Bonavina L, Rosman C, Garcia JR, et al. Minimally invasive versus open oesophagectomy for patients with oesophageal cancer: a multicentre, open-label, randomised controlled trial. Lancet. 2012;379:1887–92.
Booka E, Takeuchi H, Nishi T, Matsuda S, Kaburagi T, Fukuda K, et al. The impact of postoperative complications on survivals after esophagectomy for esophageal cancer. Medicine (Baltimore). 2015;94:e1369.
Markar SR, Arya S, Karthikesalingam A, Hanna GB. Technical factors that affect anastomotic integrity following esophagectomy: systematic review and meta-analysis. Ann Surg Oncol. 2013;20:4274–81.
Zehetner J, DeMeester SR, Alicuben ET, Oh DS, Lipham JC, Hagen JA, et al. Intraoperative assessment of perfusion of the gastric graft and correlation with anastomotic leaks after esophagectomy. Ann Surg. 2015;262:74–8.
Ishizawa T, Saiura A, Kokudo N. Clinical application of indocyanine green-fluorescence imaging during hepatectomy. Hepatobiliary Surg Nutr. 2016;5:322–8.
Karampinis I, Ronellenfitsch U, Mertens C, Gerken A, Hetjens S, Post S, et al. Indocyanine green tissue angiography affects anastomotic leakage after esophagectomy. A retrospective, case-control study. Int J Surg. 2017;48:210–4.
Van Daele E, Van Nieuwenhove Y, Ceelen W, Vanhove C, Braeckman BP, Hoorens A, et al. Near-infrared fluorescence guided esophageal reconstructive surgery: a systematic review. World J Gastrointest Oncol. 2019;11:250–63.
Shimada Y, Okumura T, Nagata T, Sawada S, Matsui K, Hori T, et al. Usefulness of blood supply visualization by indocyanine green fluorescence for reconstruction during esophagectomy. Esophagus. 2011;8:259–66.
Kumagai Y, Ishiguro T, Haga N, Kuwabara K, Kawano T, Ishida H. Hemodynamics of the reconstructed gastric tube during esophagectomy: assessment of outcomes with indocyanine green fluorescence. World J Surg. 2014;38:138–43.
Rino Y, Yukawa N, Sato T, Yamamoto N, Tamagawa H, Hasegawa S, et al. Visualization of blood supply route to the reconstructed stomach by indocyanine green fluorescence imaging during esophagectomy. BMC Med Imaging. 2014;14:18.
Campbell C, Reames MK, Robinson M, Symanowski J, Salo JC. Conduit vascular evaluation is associated with reduction in anastomotic leak after esophagectomy. J Gastrointest Surg. 2015;19:806–12.
Yukaya T, Saeki H, Kasagi Y, Nakashima Y, Ando K, Imamura Y, et al. Indocyanine green fluorescence angiography for quantitative evaluation of gastric tube perfusion in patients undergoing esophagectomy. J Am Coll Surg. 2015;221:e37-42.
Kitagawa H, Namikawa T, Munekage M, Akimori T, Kobayashi M, Hanazaki K. Visualization of the stomach’s arterial networks during esophageal surgery using the HyperEye medical system. Anticancer Res. 2015;35:6201–5.
Koyanagi K, Ozawa S, Oguma J, Kazuno A, Yamazaki Y, Ninomiya Y, et al. Blood flow speed of the gastric conduit assessed by indocyanine green fluorescence: new predictive evaluation of anastomotic leakage after esophagectomy. Medicine (Baltimore). 2016;95:e4386.
Dalton BGA, Ali AA, Crandall M, Awad ZT. Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy. Am J Surg. 2018;216:524–7.
Ohi M, Toiyama Y, Mohri Y, Saigusa S, Ichikawa T, Shimura T, et al. Prevalence of anastomotic leak and the impact of indocyanine green fluorescein imaging for evaluating blood flow in the gastric conduit following esophageal cancer surgery. Esophagus. 2017;14:351–9.
Kumagai Y, Hatano S, Sobajima J, Ishiguro T, Fukuchi M, Ishibashi KI, et al. Indocyanine green fluorescence angiography of the reconstructed gastric tube during esophagectomy: efficacy of the 90-second rule. Dis Esophagus. 2018. https://doi.org/10.1093/dote/doy052.
Noma K, Shirakawa Y, Kanaya N, Okada T, Maeda N, Ninomiya T, et al. Visualized evaluation of blood flow to the gastric conduit and complications in esophageal reconstruction. J Am Coll Surg. 2018;226:241–51.
Ishige F, Nabeya Y, Hoshino I, Takayama W, Chiba S, Arimitsu H, et al. Quantitative assessment of the blood perfusion of the gastric conduit by indocyanine green imaging. J Surg Res. 2019;234:303–10.
Kitagawa H, Namikawa T, Iwabu J, Yokota K, Uemura S, Munekage M, et al. Correlation between indocyanine green visualization time in the gastric tube and postoperative endoscopic assessment of the anastomosis after esophageal surgery. Surg Today. 2020;50:1375–82.
Talavera-Urquijo E, Parise P, Palucci M, Olivari G, Turi S, Cossu A, et al. Perfusion speed of indocyanine green in the stomach before tubulization is an objective and useful parameter to evaluate gastric microcirculation during Ivor-Lewis esophagectomy. Surg Endosc. 2020;34:5649–59.
Slooter MD, de Bruin DM, Eshuis WJ, Veelo DP, van Dieren S, Gisbertz SS, et al. Quantitative fluorescence-guided perfusion assessment of the gastric conduit to predict anastomotic complications after esophagectomy. Dis Esophagus. 2021;34:doaa100. https://doi.org/10.1093/dote/doaa100.
Koyanagi K, Ozawa S, Ninomiya Y, Oguma J, Kazuno A, Yatabe K, et al. Association between indocyanine green fluorescence blood flow speed in the gastric conduit wall and superior mesenteric artery calcification: predictive significance for anastomotic leakage after esophagectomy. Esophagus. 2021;18:248–57.
Yamaguchi K, Kumagai Y, Saito K, Hoshino A, Tokairin Y, Kawada K, et al. The evaluation of the gastric tube blood flow by indocyanine green fluorescence angiography during esophagectomy: a multicenter prospective study. Gen Thorac Cardiovasc Surg. 2021;69:1118–24.
Kitagawa H, Namikawa T, Iwabu J, Hanazaki K. Gastric tube reconstruction with superdrainage using indocyanine green fluorescence during esophagectomy. In Vivo. 2017;31:1019–21.
Handa T, Katare RG, Nishimori H, Wariishi S, Fukutomi T, Yamamoto M, et al. New device for intraoperative graft assessment: HyperEye charge-coupled device camera system. Gen Thorac Cardiovasc Surg. 2010;58:68–77.
Yamamoto M, Orihashi K, Nishimori H, Wariishi S, Fukutomi T, Kondo N, et al. Indocyanine green angiography for intra-operative assessment in vascular surgery. Eur J Vasc Endovasc Surg. 2012;43:426–32.
Hokimoto N, Sugimoto T, Namikawa T, Funakoshi T, Oki T, Ogawa M, et al. A novel color fluorescence navigation system for intraoperative transcutaneous lymphatic mapping and resection of sentinel lymph nodes in breast cancer: comparison with the combination of gamma probe scanning and visible dye methods. Oncology. 2018;94:99–106.
Nitori N, Deguchi T, Kubota K, Yoshida M, Kato A, Kojima M, et al. Successful treatment of non-occlusive mesenteric ischemia (NOMI) using the HyperEye Medical System™ for intraoperative visualization of the mesenteric and bowel circulation: report of a case. Surg Today. 2014;44:359–62.
Kubota K, Yoshida M, Kuroda J, Okada A, Ohta K, Kitajima M. Application of the HyperEye medical system for esophageal cancer surgery: a preliminary report. Surg Today. 2013;43:215–20.
Mine S, Watanabe M, Okamura A, Imamura Y, Kajiyama Y, Sano T. Superior thoracic aperture size is significantly associated with cervical anastomotic leakage after esophagectomy. World J Surg. 2017;41:2598–604.
Sucher R, Athanasios A, Köhler H, Wagner T, Brunotte M, Lederer A, et al. Hyperspectral Imaging (his) in anatomic left liver resection. Int J Surg Case Rep. 2019;62:108–11.
Köhler H, Jansen-Winkeln B, Maktabi M, Barberio M, Takoh J, Holfert N, et al. Evaluation of hyperspectral imaging (HSI) for the measurement of ischemic conditioning effects of the gastric conduit during esophagectomy. Surg Endosc. 2019;33:3775–82.
Barberio M, Felli E, Seyller E, Longo F, Chand M, Gockel I, et al. Quantitative fluorescence angiography versus hyperspectral imaging to assess bowel ischemia: a comparative study in enhanced reality. Surgery. 2020;168:178–84.
Tsutsumi R, Ikeda T, Nagahara H, Saeki H, Nakashima Y, Oki E, et al. Efficacy of novel multispectral imaging device to determine anastomosis for esophagogastrostomy. J Surg Res. 2019;242:11–22.
Jansen SM, de Bruin DM, van Berge Henegouwen MI, Bloemen PR, Strackee SD, Veelo DP, et al. Quantitative change of perfusion in gastric tube reconstruction by sidestream dark field microscopy (SDF) after esophagectomy, a prospective in-vivo cohort study. Eur J Surg Oncol. 2021;47:1034–41.
Milstein DMJ, Ince C, Gisbertz SS, Boateng KB, Geerts BF, Hollmann MW, et al. Laser speckle contrast imaging identifies ischemic areas on gastric tube reconstructions following esophagectomy. Medicine (Baltimore). 2016;95:e3875.
Yoshimi F, Asato Y, Ikeda S, Okamoto K, Komuro Y, Imura J, et al. Using the supercharge technique to additionally revascularize the gastric tube after a subtotal esophagectomy for esophageal cancer. Am J Surg. 2006;191:284–7.
Saeki H, Morita M, Harada N, Egashira A, Oki E, Uchiyama H, et al. Esophageal replacement by colon interposition with microvascular surgery for patients with thoracic esophageal cancer: the utility of superdrainage. Dis Esophagus. 2013;26:50–6.
Fujioka M, Hayashida K, Fukui K, Ishiyama S, Saijo H, Taniguchi K. Venous superdrained gastric tube pull-up procedure for hypopharyngeal and cervical esophageal reconstruction reduces postoperative anastomotic leakage and stricture. Dis Esophagus. 2017;30:1–6.
Kono K, Sugai H, Omata H, Fujii H. Transient bloodletting of the short gastric vein in the reconstructed gastric tube improves gastric microcirculation during esophagectomy. World J Surg. 2007;31:780–4.
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We would like to thank Editage (www.editage.com) for editing the English language of this article.
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Kitagawa, H., Yokota, K., Marui, A. et al. Near-infrared fluorescence imaging with indocyanine green to assess the blood supply of the reconstructed gastric conduit to reduce anastomotic leakage after esophagectomy: a literature review. Surg Today 53, 399–408 (2023). https://doi.org/10.1007/s00595-022-02474-y
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DOI: https://doi.org/10.1007/s00595-022-02474-y