Near-infrared fluorescence image-guided surgery helps surgeons to see beyond the classical eye vision. Over the last few years, we have witnessed a revolution which has begun in the field of image-guided surgery.
Purpose, and Research design
Fluorescence technology using indocyanine green (ICG) has shown promising results in many organs, and in this review article, we wanted to discuss the 6 main domains where fluorescence image-guided surgery is currently used for esophageal and gastric cancer surgery.
Study sample and data collection
Visualization of lymphatic vessels, tumor localization, fluorescence angiography for anastomotic evaluation, thoracic duct visualization, tracheal blood flow analysis, and sentinel node biopsy are discussed.
Conclusions
It seems that this technology has already found its place in surgery. However, new possibilities and research avenues in this area will probably make it even more important in the near future.
KitaiTInomotoTMiwaMShikayamaT. Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer. 2005;12:211-215.
2.
KirchherrAKBrielAMäderK. Stabilization of indocyanine green by encapsulation within micellar systems. Mol Pharm. 2009;6(2):480-491. doi:10.1021/mp8001649.
3.
SasakoMSanoTYamamotoS, et al.D2 lymphadenectomy alone or with para-aortic nodal dissection for gastric cancer. N Engl J Med. 2008;359(5):453-462.
4.
SongunIPutterHKranenbargEMKSasakoMvan de VeldeCJH. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol. 2010;11(5):439-449.
5.
Herrera-AlmarioGPataneMSarkariaIStrongVE. Initial report of near-infrared fluorescence imaging as an intraoperative adjunct for lymph node harvesting during robot-assisted laparoscopic gastrectomy. J Surg Oncol. 2016;113(7):768-770.
6.
LanY-THuangK-HChenP-H, et al.A pilot study of lymph node mapping with indocyanine green in robotic gastrectomy for gastric cancer. SAGE Open Med. 2017;5:2050312117727444.
7.
ChenQYXieJWZhongQ, et al.Safety and efficacy of indocyanine green tracer-guided lymph node dissection during laparoscopic radical gastrectomy in patients with gastric cancer: A randomized clinical trial. JAMA Surg. 2020;155(4):300-311.
8.
BaiocchiGLMolfinoSMolteniB, et al.Fluorescence-guided lymphadenectomy in gastric cancer: a prospective western series. Updates Surg. 2020;72(3):761-772.
9.
PolomWMarkuszewskiMRhoYSMatuszewskiM. Use of invisible near infrared light fluorescence with indocyanine green and methylene blue in urology. Part 2. Cent European J Urol. 2014;67(3):310-313.
10.
RohCKChoiSSeoWJChoMSonTKimH-IHyungWJ. Indocyanine green fluorescence lymphography during gastrectomy after initial endoscopic submucosal dissection for early gastric cancer. British Journal of Surgery. 2020;107(6):712-719. https://doi.org/10.1002/bjs.11438
11.
ChoiHJKimJMRyuJM, et al.Patterns of axillary lymph node metastasis in breast cancer: A prospective single-center study. J Breast Cancer. 2018;21(4):447-452.
12.
TummersQRJGBoogerdLSFDe SteurWO, et al.Near-infrared fluorescence sentinel lymph node detection in gastric cancer: A pilot study Clinical Trials Study. World J Gastroenterol. 2016;22(13):3644-3651.
13.
YaguchiYIchikuraTOnoS, et al.How should tracers be injected to detect for sentinel nodes in gastric cancer-submucosally from inside or subserosally from outside of the stomach?J Exp Clin Cancer Res. 2008;27(1):79.
14.
CianchiFIndennitateGPaoliB, et al.The clinical value of fluorescent lymphography with indocyanine green during robotic surgery for gastric cancer: A matched cohort study. J Gastrointest Surg. 2020;24(10):2197-2203.
15.
LiuMXingJXuK, et al.Application of near-infrared fluorescence imaging with indocyanine green in totally laparoscopic distal gastrectomy. J Gastric Cancer. 2020;20(3):290-299.
16.
UshimaruYOmoriTFujiwaraY, et al.The feasibility and safety of preoperative fluorescence marking with indocyanine green (ICG) in laparoscopic gastrectomy for gastric cancer. J Gastrointest Surg. 2019;23(3):468-476.
17.
TanakaCKandaMFunasakaK, et al.Detection of indocyanine green fluorescence to determine tumor location during laparoscopic gastrectomy for gastric cancer: Results of a prospective study. Asian J Endosc Surg. 2020;13(2):160-167.
18.
HyunJHKimSKKimKG, et al.A novel endoscopic fluorescent band ligation method for tumor localization. Surg Endosc. 2016;30(10):4659-4663.
19.
de ValkKSDekenMMSchaapDP, et al.Dose-finding study of a CEA-targeting agent, SGM-101, for intraoperative fluorescence imaging of colorectal cancer. Ann Surg Oncol. 2020;28(3):1832-1844.
20.
DegettTHAndersenHSGögenurI. Indocyanine green fluorescence angiography for intraoperative assessment of gastrointestinal anastomotic perfusion: a systematic review of clinical trials. Langenbeck's Arch Surg. 2016;401(6):767-775. doi:10.1007/s00423-016-1400-9.
21.
KassisESKosinskiASRossPKoppesKEDonahueJMDanielVC. Predictors of anastomotic leak after esophagectomy: An analysis of the society of thoracic surgeons general thoracic database. Ann Thorac Surg. 2013;96(6):1919-1926.
22.
BiereSSAYMaasKWCuestaMAVan Der PeetDL. Cervical or thoracic anastomosis after esophagectomy for cancer: A systematic review and meta-analysis. Dig Surg. 2011;28(1):29-35.
23.
SauvanetAMarietteCThomasP, et al.Mortality and morbidity after resection for adenocarcinoma of the gastroesophageal junction: Predictive factors. J Am Coll Surg. 2005;201(2):253-262.
24.
SunpaweravongSRuangsinSLaohawiriyakamolSMahattanobonSGeaterA. Prediction of major postoperative complications and survival for locally advanced esophageal carcinoma patients. Asian J Surg. 2012;35(3):104-109.
25.
HagaYWadaYTakeuchiHIkejiriKIkenagaM. Prediction of anastomotic leak and its prognosis in digestive surgery. World J Surg. 2011;35(4):716-722.
26.
KimKMAnJYKimHICheongJHHyungWJNohSH. Major early complications following open, laparoscopic and robotic gastrectomy. Br J Surg. 2012;99(12):1681-1687.
27.
KimMCKimWKimHH, et al.Risk factors associated with complication following laparoscopy-assisted gastrectomy for gastric cancer: A large-scale Korean multicenter study. Ann Surg Oncol. 2008;15(10):2692-2700.
28.
KitanoSShiraishiNUyamaI, et al.A multicenter study on oncologic outcome of laparoscopic gastrectomy for early cancer in Japan. Ann Surg. 2007;245(1):68-72.
29.
NagasakoYSatohSIsogakiJInabaKTaniguchiKUyamaI. Impact of anastomotic complications on outcome after laparoscopic gastrectomy for early gastric cancer. Br J Surg. 2012;99(6):849-854.
30.
LeeKGLeeHJYangJY, et al.Risk factors associated with complication following gastrectomy for gastric cancer: Retrospective analysis of prospectively collected data based on the Clavien-Dindo system. J Gastrointest Surg. 2014;18(7):1269-1277.
31.
GalloroG. Staple-line leak after sleve gastrectomy in obese patients: A hot topic in bariatric surgery. World J Gastrointest Endosc. 2015;7(9):843-846.
32.
Abou RachedABasileMEl MasriH. Gastric leaks post sleeve gastrectomy: Review of its prevention and management. World J Gastroenterol. 2014;20(38):13904-13910.
33.
SakranNGoiteinDRazielA, et al.Gastric leaks after sleeve gastrectomy: A multicenter experience with 2,834 patients. Surg Endosc. 2013;27(1):240-245.
34.
MarcheseMRomanoLGiulianiA, et al.Corrigendum to “A case of intrasplenic displacement of an endoscopic double-pigtailstent as a treatment for laparoscopic sleeve gastrectomy leak” [(International Journal of Surgery Case Reports) (2018) 53 (367–369). Int J Sur Case Rep. 2019;56:49.
35.
JansenSMde BruinDMvan Berge HenegouwenMIStrackeeSDVeeloDPvan LeeuwenTGGisbertzSS. Optical techniques for perfusion monitoring of the gastric tube after esophagectomy: A review of technologies and thresholds, Diseases of the Esophagus. 2018;31(6):dox161. https://doi.org/10.1093/dote/dox161
36.
MilsteinDMJInceCGisbertzSS, et al.Laser speckle contrast imaging identifies ischemic areas on gastric tube reconstructions following esophagectomy. Medicine. 2016;95(25):e3875.
37.
LinderGHedbergJBjörckMSundbomM. Perfusion of the gastric conduit during esophagectomy. Dis Esophagus. 2017;30(1):143-149.
38.
PhamTHPerryKAEnestvedtCK, et al.Decreased conduit perfusion measured by spectroscopy is associated with anastomotic complications. Ann Thorac Surg. 2011;91(2):380-385.
39.
TsekovCBelyaevOTcholakovOTcherveniakovA. Intraoperative Doppler Assessment of Gastric Tube Perfusion in Esophagogastroplasty. J Surg Res. 2006;132(1):98-103.
40.
KoyanagiKOzawaSNinomiyaY, 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. 2020;18(2):248-257.
41.
ThammineediSRPatnaikSCSaksenaARRamalingamPRNusrathS. The utility of indocyanine green angiography in the assessment of perfusion of gastric conduit and proximal esophageal stump against visual assessment in patients undergoing esophagectomy: A prospective study. Indian J Surg Oncol. 2020;11(4):684-691.
42.
NerupNSvendsenMBSSvendsenLBAchiamMP. Feasibility and usability of real-time intraoperative quantitative fluorescent-guided perfusion assessment during resection of gastroesophageal junction cancer. Langenbeck's Arch Surg. 2020;405(2):215-222.
43.
IshigeFNabeyaYHoshinoI, et al.Quantitative assessment of the blood perfusion of the gastric conduit by indocyanine green imaging. J Surg Res. 2019;234:303-310.
44.
DaltonBGAAliAACrandallMAwadZT. Near infrared perfusion assessment of gastric conduit during minimally invasive Ivor Lewis esophagectomy. Am J Surg. 2018;216(3):524-527.
45.
KitagawaHNamikawaTIwabuJ, et al.Assessment of the blood supply using the indocyanine green fluorescence method and postoperative endoscopic evaluation of anastomosis of the gastric tube during esophagectomy. Surg Endosc. 2018;32(4):1749-1754.
46.
KumagaiYHatanoSSobajimaJ, et al.Indocyanine green fluorescence angiography of the reconstructed gastric tube during esophagectomy: Efficacy of the 90-second rule. Dis Esophagus. 2018;31(12):1–4.
47.
NomaKShirakawaYKanayaN, et al.Visualized evaluation of blood flow to the gastric conduit and complications in esophageal reconstruction. J Am Coll Surg. 2018;226(3):241-251.
48.
KarampinisIRonellenfitschUMertensC, et al.Indocyanine green tissue angiography affects anastomotic leakage after esophagectomy. A retrospective, case-control study. Int J Surg. 2017;48:210-214.
49.
OhiMToiyamaYMohriY, 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(4):351-359.
50.
SchlottmannFPattiMG. Evaluation of gastric conduit perfusion during esophagectomy with indocyanine green fluorescence imaging. J Laparoendosc Adv Surg Tech. 2017;27(12):1305-1308.
51.
KoyanagiKOzawaSOgumaJ, et al.Blood flow speed of the gastric conduit assessed by indocyanine green fluorescence: New predictive evaluation of anastomotic leakage after esophagectomy. Medicine. 2016;95(30):e4386.
52.
CampbellCReamesMKRobinsonMSymanowskiJSaloJC. Conduit Vascular Evaluation is Associated with Reduction in Anastomotic Leak After Esophagectomy. J Gastrointest Surg. 2015;19(5):806-812.
53.
KamiyaKUnnoNMiyazakiS, et al.Quantitative assessment of the free jejunal graft perfusion. J Surg Res. 2015;194(2):394-399.
54.
YukayaTSaekiHKasagiY, et al.Indocyanine green fluorescence angiography for quantitative evaluation of gastric tube perfusion in patients undergoing esophagectomy. J Am Coll Surg. 2015;221(2):e37-e42.
55.
ZehetnerJDeMeesterSRAlicubenET, et al.Intraoperative assessment of perfusion of the gastric graft and correlation with anastomotic leaks after esophagectomy. Ann Surg. 2015;262(1):74-78.
56.
KumagaiYIshiguroTHagaNKuwabaraKKawanoTIshidaH. Hemodynamics of the reconstructed gastric tube during esophagectomy: Assessment of outcomes with indocyanine green fluorescence. World J Surg. 2014;38(1):138-143.
57.
SarkariaISBainsMSFinleyDJ, et al.Intraoperative near-infrared fluorescence imaging as an adjunct to robotic-assisted minimally invasive esophagectomy. Innovat Tech Tech CardioThorac Vasc Surg. 2014;9(5):391-393.
58.
RinoYYukawaNSatoT, et al.Visualization of blood supply route to the reconstructed stomach by indocyanine green fluorescence imaging during esophagectomy. BMC Med Imag. 2014;14:18.
59.
PachecoPEHillSMHenriquesSMPaulsenJKAndersonRC. The novel use of intraoperative laser-induced fluorescence of indocyanine green tissue angiography for evaluation of the gastric conduit in esophageal reconstructive surgery. Am J Surg. 2013;205(3):349-352.
60.
KubotaKYoshidaMKurodaJOkadaAOhtaKKitajimaM. Application of the HyperEye medical system for esophageal cancer surgery: A preliminary report. Surg Today. 2013;43(2):215-220.
61.
SlooterMDEshuisWJCuestaMAGisbertzSSvan Berge HenegouwenMI. Fluorescent imaging using indocyanine green during esophagectomy to prevent surgical morbidity: A systematic review and meta-analysis. J Thorac Dis. 2019;11(suppl 5):S755-S765.
62.
PurichKDangJTPoonjaA, et al.Intraoperative fluorescence imaging with indocyanine green in hepatic resection for malignancy: A systematic review and meta-analysis of diagnostic test accuracy studies. Surg Endosc. 2020;34(7):2891-2903.
63.
ShimadaYOkumuraTNagataT, et al.Usefulness of blood supply visualization by indocyanine green fluorescence for reconstruction during esophagectomy. Esophagus. 2011;8(4):259-266.
64.
MoriMShutoKHiranoA, et al.A novel parameter identified using indocyanine green fluorescence angiography may contribute to predicting anastomotic leakage in gastric cancer surgery. World J Surg. 2020;44(8):2699-2708.
65.
HuhYJLeeHJKimTH, et al.Efficacy of assessing intraoperative bowel perfusion with near-infrared camera in laparoscopic gastric cancer surgery. J Laparoendosc Adv Surg Tech. 2019;29(4):476-483.
66.
MurawaDHünerbeinMSpychałaANowaczykPPołomKMurawaP. Indocyanine green angiography for evaluation of gastric conduit perfusion during esophagectomy-first experience. Acta Clin Belg. 2012;112(4):275-280.
67.
NishikawaKFujitaTYudaM, et al.Quantitative assessment of blood flow in the gastric conduit with thermal imaging for esophageal reconstruction. Ann Surg. 2020;271(6):1087-1094.
68.
Van DaeleEVan NieuwenhoveYCeelenW, et al.Near-infrared fluorescence guided esophageal reconstructive surgery: A systematic review. World J Gastrointest Oncol. 2019;11(3):250-263.
69.
DianaMNollEDiemunschP, et al.Enhanced-reality video fluorescence: A real-time assessment of intestinal viability. Ann Surg. 2014;259(4):700-707.
70.
DianaMHalvaxPDallemagneB, et al.Real-time navigation by fluorescence-based enhanced reality for precise estimation of future anastomotic site in digestive surgery. Surg Endosc. 2014;28(11):3108-3118.
71.
DianaMAgnusVHalvaxP, et al.Intraoperative fluorescence-based enhanced reality laparoscopic real-time imaging to assess bowel perfusion at the anastomotic site in an experimental model. Br J Surg. 2015;102(2):e169-e176.
72.
van ManenLHandgraafHJMDianaM, et al.A practical guide for the use of indocyanine green and methylene blue in fluorescence-guided abdominal surgery. J Surg Oncol. 2018;118(2):283-300.
73.
CharalabopoulosAKordzadehASdralisELorenziBAhmadF. Thoracoscopic total esophagogastrectomy with supercharged colon interposition for the treatment of esophageal adenocarcinoma in situs inversus. Acta Chir Belg. 2019;119(4):259-262.
74.
SugimuraKMiyataHShinnoN, et al.Indocyanine green fluorescence imaging of the tracheal blood flow during esophagectomy. J Surg Res. 2019;241:1-7.
75.
FujitaHKawaharaHHidakaMNaganoTYoshimatsuH. An experimental study on viability of the devascularized trachea. Jpn J Surg. 1988;18(1):77-83.
76.
VecchiatoMMartinoASponzaM, et al.Thoracic duct identification with indocyanine green fluorescence during minimally invasive esophagectomy with patient in prone position. Dis Esophagus. 2020;33(12):doaa030.
77.
KaburagiTTakeuchiHOyamaT, et al.Intraoperative fluorescence lymphography using indocyanine green in a patient with chylothorax after esophagectomy: report of a case. Surg Today. 2013;43(2):206–210.
78.
MatsutaniTHirakataANomuraT, et al.Transabdominal Approach for Chylorrhea after Esophagectomy by Using Fluorescence Navigation with Indocyanine Green. Case Rep Surg. 2014;2014:464017.
79.
KamiyaKUnnoNKonnoH. Intraoperative indocyanine green fluorescence lymphography, a novel imaging technique to detect a chyle fistula after an esophagectomy: Report of a case. Surg Today. 2009;39(5):421-424.
80.
De ManzoniGMarrelliDBaiocchiGL, et al.The Italian Research Group for Gastric Cancer (GIRCG) guidelines for gastric cancer staging and treatment: 2015. Gastric Cancer. 2017;20(1):20-30.
81.
Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer. 2020;24(1):1-21
82.
CardosoRBocicariuADixonM, et al.What is the accuracy of sentinel lymph node biopsy for gastric cancer? a systematic review. Gastric Cancer. 2012;15(suppl 1):S48-S59.
83.
WangZDongZYChenJQLiuJL. Diagnostic value of sentinel lymph node biopsy in gastric cancer: A meta-analysis. Ann Surg Oncol. 2012;19(5):1541-1550.
84.
NimuraHNarimiyaNMitsumoriNYamazakiYYanagaKUrashimaM. Infrared ray electronic endoscopy combined with indocyanine green injection for detection of sentinel nodes of patients with gastric cancer. Br J Surg. 2004;91(5):575-579.
85.
SolteszEGKimSKimSW, et al.Sentinel lymph node mapping of the gastrointestinal tract by using invisible light. Ann Surg Oncol. 2006;13(3):386-396.
86.
KusanoMTajimaYYamazakiKKatoMWatanabeMMiwaM. Sentinel node mapping guided by indocyanine green fluorescence imaging: a new method for sentinel node navigation surgery in gastrointestinal cancer. Dig Surg. 2008;25(2):103-108.
87.
BalaguéCGomezI. Preoperative and intraoperative lymphatic mapping for sentinel node biopsy in cancers of the gastrointestinal Tract. In: Atlas of Lymphoscintigraphy and Sentinel Node Mapping. Springer, Cham; 2020.
88.
LeeYJHaWSParkSTChoiSKHongSCParkJW. Which biopsy method is more suitable between a basin dissection and pick-up biopsy for sentinel nodes in laparoscopic sentinel-node navigation surgery (LSNNS) for gastric cancer?J Laparoendosc Adv Surg Tech. 2008;18(3):357-363.
89.
VuijkFAHillingDEMieogJSDVahrmeijerAL. Fluorescent-guided surgery for sentinel lymph node detection in gastric cancer and carcinoembryonic antigen targeted fluorescent-guided surgery in colorectal and pancreatic cancer. J Surg Oncol. 2018;118(2):315-323.
HagensERCvan Berge HenegouwenMIGisbertzSS. Distribution of lymph node metastases in esophageal carcinoma patients undergoing upfront surgery: A systematic review. Cancers. 2020;12(6):1592.
92.
TachibanaMKinugasaSShibakitaM, et al.Surgical treatment of superficial esophageal cancer. Langenbeck's Arch Surg. 2006;391(4):304-321.
93.
AndoNOzawaSKitagawaYShinozawaYKitajimaM. Improvement in the results of surgical treatment of advanced squamous esophageal carcinoma during 15 consecutive years. Ann Surg. 2000;232(2):225-232.
94.
YasudaSShimadaHChinoO, et al.Sentinel lymph node detection with Tc-99m tin colloids in patients with esophagogastric cancer. Jpn J Clin Oncol. 2003;33(2):68-72.
95.
HayashiHTangokuASugaK, et al.CT lymphography-navigated sentinel lymph node biopsy in patients with superficial esophageal cancer. Surgery. 2006;139(2):224-235.
96.
TangokuASeikeJNakanoK, et al.Current status of sentinel lymph node navigation surgery in breast and gastrointestinal tract. J Med Invest. 2007;54(1-2):1-18.
97.
KitagawaYFujiiHMukaiM, et al.[The validity of the sentinel node concept in gastrointestinal cancers]. Nihon Geka Gakkai Zasshi. 2000;101(3):315-319.
98.
SchlottmannFBarbettaAMungoBLidorAOMolenaD. Identification of the Lymphatic Drainage Pattern of Esophageal Cancer with Near-Infrared Fluorescent Imaging. J Laparoendosc Adv Surg Tech A. 2017;27(3):268–271.
99.
YuasaYSeikeJYoshidaT, et al.Sentinel lymph node biopsy using intraoperative indocyanine green fluorescence imaging navigated with preoperative CT lymphography for superficial esophageal cancer. Ann Surg Oncol. 2012;19(2):486-493.
100.
HelminenOMrenaJSihvoESihvoE. Near-infrared image-guided lymphatic mapping in minimally invasive oesophagectomy of distal oesophageal cancer. Eur J Cardiothorac Surg. 2017;52(5):952-957.
101.
HacheyKJGilmoreDMArmstrongKW, et al.Safety and feasibility of near-infrared image-guided lymphatic mapping of regional lymph nodes in esophageal cancer. J Thorac Cardiovasc Surg. 2016;152(2):546-554.
102.
Jimenez-LilloJVillegas-TovarEMomblan-GarciaD, et al.Performance of indocyanine-green imaging for sentinel lymph node mapping and lymph node metastasis in esophageal cancer: Systematic review and meta-analysis. Ann Surg Oncol. 2021;28(9):4869-4877. Available from: http://europepmc.org/abstract/MED/33515138.
