Indocyanine green and near-infrared fluorescence imaging in minimally invasive gastric cancer surgery: a narrative review

Abstract

Background: The popularity of minimally invasive surgery for gastric cancer has been on the rise due to its advantages in faster recovery and improved outcomes. However, the lack of tactile sensation poses challenges for tumor identification and anatomical recognition. Indocyanine green (ICG) with near-infrared (NIR) fluorescence imaging has emerged as a potential solution to address these challenges. This review summarizes the current status, limitations, and future prospects of ICG and NIR fluorescence imaging in minimally invasive surgery for gastric cancer. Search strategy: This narrative review searched the PubMed database for relevant articles related to ICG and NIR fluorescence imaging in minimally invasive gastric cancer surgery, published through 2023. The search criteria comprised “indocyanine green”, “ICG”, “near-infrared fluorescence imaging”, “gastric cancer”, “gastrectomy”, and “minimally invasive surgery”. Findings: ICG with NIR fluorescence imaging offers three main applications in gastric cancer surgery. Firstly, it aids in real-time intraoperative tumor identification when injected locally around the tumor, surpassing traditional tattooing techniques. Secondly, ICG facilitates lymph node mapping, particularly in identifying sentinel lymph nodes, which could reduce unnecessary lymphadenectomy. Thirdly, ICG angiography enables the assessment of blood perfusion during reconstructive surgery, evaluating anastomosis sites and potentially reducing anastomotic leakage risk. Conclusions: ICG and NIR fluorescence imaging have shown promising advancements in enhancing the precision and safety of minimally invasive gastric cancer surgery. However, standardized analysis methods and further prospective studies are needed to fully establish their clinical significance. Overall, ICG and NIR fluorescence imaging hold potential as valuable tools to improve patient outcomes in minimally invasive gastric cancer surgery.

Keywords

Indocyanine green / near-infrared fluorescence imaging / gastric cancer / gastrectomy / minimally invasive surgery

References

[1] Kim HH,Kim MC.Effect of laparoscopic distal gastrectomy vs open distal gastrectomy on long-term survival among patients with stage I gastric cancer: the KLASS-01 randomized clinical trial.JAMA Oncol2019;5:506-13 PMCID:PMC6459124

[2] Hamed OH,Kimchi ET.Minimally invasive surgery in gastrointestinal cancer: benefits, challenges, and solutions for underutilization.JSLS2014;18:e2014.00134 PMCID:PMC4254473

[3] Alander JT,Laakso A.A review of indocyanine green fluorescent imaging in surgery.Int J Biomed Imaging2012;2012:940585 PMCID:PMC3346977

[4] Paumgartner G.The handling of indocyanine green by the liver.Schweiz Med Wochenschr1975;105:1-30

[5] Kitagawa H,Marui A,Kobayashi M.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 Today2023;53:399-408

[6] Quan YH,Kim HK.Fluorescence Image-Based Evaluation of Gastric Tube Perfusion during Esophagogastrostomy.Korean J Thorac Cardiovasc Surg2020;53:178-83 PMCID:PMC7409886

[7] Iwamoto M,Kawamura J.A narrative review of the usefulness of indocyanine green fluorescence angiography for perfusion assessment in colorectal surgery.Cancers2022;14:5623 PMCID:PMC9688558

[8] Majlesara A,Hafezi M.Indocyanine green fluorescence imaging in hepatobiliary surgery.Photodiagnosis Photodyn Ther2017;17:208-15

[9] Serban D,Davitoiu D.Systematic review of the role of indocyanine green near-infrared fluorescence in safe laparoscopic cholecystectomy (review).Exp Ther Med2022;23:187 PMCID:PMC8764893

[10] Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2021 (6th edition).Gastric Cancer2023;26:1-25 PMCID:PMC9813208

[11] Jeong SH,Min JS.Intraoperative tumor localization of early gastric cancers.J Gastric Cancer2021;21:4-15 PMCID:PMC8020001

[12] Barberio M,Laracca GG.Endoscopic preoperative tattooing and marking in the gastrointestinal tract: a systematic review of alternative methods.J Laparoendosc Adv Surg Tech A2020;30:953-61

[13] Ono H,Nihei M.[Effectiveness of indocyanine green fluorescence in endoscopic marking in gastric cancer surgery:a feasibility study for replacing India ink].Nihon Shokakibyo Gakkai Zasshi2018;115:385-93

[14] Ushimaru Y,Fujiwara Y.The feasibility and safety of preoperative fluorescence marking with indocyanine green (ICG) in laparoscopic gastrectomy for gastric cancer.J Gastrointest Surg2019;23:468-76

[15] Omori T,Shinno N.Safety and efficacy of preoperative indocyanine green fluorescence marking in laparoscopic gastrectomy for proximal gastric and esophagogastric junction adenocarcinoma (ICG MAP study).Langenbecks Arch Surg2022;407:3387-96

[16] Tanaka C,Funasaka K.Detection of indocyanine green fluorescence to determine tumor location during laparoscopic gastrectomy for gastric cancer: results of a prospective study.Asian J Endosc Surg2020;13:160-7

[17] Cho M,Park SH,Kim HI.Securing resection margin using indocyanine green diffusion range on gastric wall during NIR fluorescence-guided surgery in early gastric cancer patients.Cancers2022;14:5223 PMCID:PMC9658562

[18] Narihiro S,Ohdaira H.Near-infrared fluorescent clip guided gastrectomy: report of 2 cases (Case reports).Ann Med Surg2020;55:49-52 PMCID:PMC7240282

[19] Namikawa T,Hashiba M.Novel endoscopic marking clip equipped with resin-conjugated fluorescent indocyanine green during laparoscopic surgery for gastrointestinal cancer.Langenbecks Arch Surg2020;405:503-8

[20] Ryu S,Nakashima K.Usefulness of preoperative endoscopic fluorescent clip marking in laparoscopic gastrointestinal surgery.Anticancer Res2020;40:6517-23

[21] Chen X,Zhang F.Analysis of safety and efficacy of laparoscopic radical gastrectomy combined with or without indocyanine green tracer fluorescence technique in treatment of gastric cancer: a retrospective cohort study.J Gastrointest Oncol2022;13:1616-25 PMCID:PMC9459186

[22] Yoon BW.The oncologic safety and accuracy of indocyanine green fluorescent dye marking in securing the proximal resection margin during totally laparoscopic distal gastrectomy for gastric cancer: a retrospective comparative study.World J Surg Oncol2022;20:26 PMCID:PMC8796580

[23] Nakanishi K,Kanda M.Preoperative indocyanine green fluorescence injection to accurately determine a proximal margin during robotic distal gastrectomy.Asian J Endosc Surg2023;16:152-6

[24] Narihiro S,Ohdaira H.Effectiveness and safety of tumor site marking with near-infrared fluorescent clips in colorectal laparoscopic surgery: a case series study.Int J Surg2020;80:74-8

[25] Kinami S,Tomita Y.Precision surgical approach with lymph-node dissection in early gastric cancer.World J Gastroenterol2019;25:1640-52 PMCID:PMC6465935

[26] Jatoi I.Omission of sentinel node biopsy for breast cancer: historical context and future perspectives on a modern controversy.Cancer2021;127:4376-83

[27] Wong SL,Kennedy EB.Sentinel lymph node biopsy and management of regional lymph nodes in melanoma: American society of clinical oncology and society of surgical oncology clinical practice guideline update summary.J Oncol Pract2018;14:242-5

[28] Lirosi MC,Ricci R.Surgical anatomy of gastric lymphatic drainage.Transl Gastroenterol Hepatol2017;2:14 PMCID:PMC5388628

[29] Ichikura T,Uchida T.Sentinel node concept in gastric carcinoma.World J Surg2002;26:318-22

[30] Ryu KW,Nam BH.Is the sentinel node biopsy clinically applicable for limited lymphadenectomy and modified gastric resection in gastric cancer? A meta-analysis of feasibility studies.J Surg Oncol2011;104:578-84

[31] Miyashiro I,Sasako M.High false-negative proportion of intraoperative histological examination as a serious problem for clinical application of sentinel node biopsy for early gastric cancer: final results of the Japan Clinical Oncology Group multicenter trial JCOG0302.Gastric Cancer2014;17:316-23

[32] Miwa K,Taniguchi K,Fujimura T.Mapping sentinel nodes in patients with early-stage gastric carcinoma.Br J Surg2003;90:178-82

[33] Kelder W,Takahashi N,van Dam GM.Sentinel node mapping with indocyanine green (ICG) and infrared ray detection in early gastric cancer: an accurate method that enables a limited lymphadenectomy.Eur J Surg Oncol2010;36:552-8

[34] Lee YJ,Park ST,Hong SC.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 A2008;18:357-63

[35] Niihara M,Nakahara T.Sentinel lymph node mapping for 385 gastric cancer patients.J Surg Res2016;200:73-81

[36] Kitagawa Y,Takagi Y.Sentinel node mapping for gastric cancer: a prospective multicenter trial in Japan.J Clin Oncol2013;31:3704-10

[37] Skubleny D,Skulsky S.Diagnostic evaluation of sentinel lymph node biopsy using indocyanine green and infrared or fluorescent imaging in gastric cancer: a systematic review and meta-analysis.Surg Endosc2018;32:2620-31

[38] Park JY,Ryu KW.Assessment of laparoscopic stomach preserving surgery with sentinel basin dissection versus standard gastrectomy with lymphadenectomy in early gastric cancer-a multicenter randomized phase III clinical trial (SENORITA trial) protocol.BMC Cancer2016;16:340 PMCID:PMC4886393

[39] An JY,Hur H.Laparoscopic sentinel node navigation surgery versus laparoscopic gastrectomy with lymph node dissection for early gastric cancer: short-term outcomes of a multicentre randomized controlled trial (SENORITA).Br J Surg2020;107:1429-39

[40] Kim YW,Yoon HM.Laparoscopic sentinel node navigation surgery for stomach preservation in patients with early gastric cancer: a randomized clinical trial.J Clin Oncol2022;40:2342-51 PMCID:PMC9287280

[41] Sherwinter DA,Bouvet M.Use of fluorescence imaging and indocyanine green for sentinel node mapping during gastric cancer surgery: results of an intercontinental Delphi survey.Surgery2022;172:S29-37 PMCID:PMC9720539

[42] Amin MB,Edge SB.The eighth edition AJCC cancer staging manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging.CA Cancer J Clin2017;67:93-9

[43] Miftode S.Misclassification of nodal stage in gastric cancer: 16 lymph nodes is not enough.Surg Exp Pathol2022;5:7

[44] Macalindong SS,Nam BH.Effect of total number of harvested lymph nodes on survival outcomes after curative resection for gastric adenocarcinoma: findings from an eastern high-volume gastric cancer center.BMC Cancer2018;18:73 PMCID:PMC5766983

[45] Chen QY,Zhong Q.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 Surg2020;155:300-11

[46] Jung MK,Roh CK.Assessment of diagnostic value of fluorescent lymphography-guided lymphadenectomy for gastric cancer.Gastric Cancer2021;24:515-25

[47] Maruri I,Cano-Valderrama O.Retrospective cohort study of laparoscopic ICG-Guided Lymphadenectomy in gastric cancer from a Western country center.Surg Endosc2022;36:8164-9

[48] Liu M,Xu K.Application of near-infrared fluorescence imaging with indocyanine green in totally laparoscopic distal gastrectomy.J Gastric Cancer2020;20:290-9 PMCID:PMC7521987

[49] Park SH,Choi JH.Near-infrared fluorescence-guided surgery using indocyanine green facilitates secure infrapyloric lymph node dissection during laparoscopic distal gastrectomy.Surg Today2020;50:1187-96

[50] Kwon IG,Kim HI.Fluorescent lymphography-guided lymphadenectomy during robotic radical gastrectomy for gastric cancer.JAMA Surg2019;154:150-8 PMCID:PMC6439673

[51] Fujimoto D,Takashima J.Indocyanine green tracer-guided radical robotic distal gastrectomy using the firefly™ system improves the quality of lymph node dissection in patients with gastric cancer.J Gastrointest Surg2023;Online ahead of print:

[52] Zhang Z,Guo Z,Qi H.Safety and efficacy of indocyanine green near-infrared fluorescent imaging-guided lymph node dissection during robotic gastrectomy for gastric cancer: a systematic review and meta-analysis.Minim Invasive Ther Allied Technol2023;1-9. Online ahead of print

[53] Park SH,Cho M,Kim HI.Prognostic impact of fluorescent lymphography on gastric cancer.Int J Surg2023;Online ahead of print:

[54] Sposito C,Conalbi V.Impact of indocyanine green fluorescence imaging on lymphadenectomy quality during laparoscopic distal gastrectomy for gastric cancer (greeneye): an adaptative, phase 2, clinical trial.Ann Surg Oncol2023;Online ahead of print:

[55] Lan YT,Chen PH.A pilot study of lymph node mapping with indocyanine green in robotic gastrectomy for gastric cancer.SAGE Open Med2017;5:2050312117727444 PMCID:PMC5570112

[56] Lee SE,Ryu KW.Sentinel node mapping and skip metastases in patients with early gastric cancer.Ann Surg Oncol2009;16:603-8

[57] Tajima Y,Masuda Y.Sentinel node mapping guided by indocyanine green fluorescence imaging in gastric cancer.Ann Surg2009;249:58-62

[58] Chen QY,Li P.Comparison of submucosal and subserosal approaches toward optimized indocyanine green tracer-guided laparoscopic lymphadenectomy for patients with gastric cancer (FUGES-019): a randomized controlled trial.BMC Med2021;19:276 PMCID:PMC8549272

[59] Li Z,Ying X.Assessment of laparoscopic distal gastrectomy after neoadjuvant chemotherapy for locally advanced gastric cancer: a randomized clinical trial.JAMA Surg2019;154:1093-101 PMCID:PMC6763995

[60] Huang ZN,Qiu WW.Assessment of indocyanine green tracer-guided lymphadenectomy in laparoscopic gastrectomy after neoadjuvant chemotherapy for locally advanced gastric cancer: results from a multicenter analysis based on propensity matching.Gastric Cancer2021;24:1355-64

[61] Puccetti F,Genova L.Applicative limitations of indocyanine green fluorescence assistance to laparoscopic lymph node dissection in total gastrectomy for cancer.Ann Surg Oncol2022;29:5875-82

[62] Lombardi PM,Nicastro V.The iGreenGO study: the clinical role of indocyanine green imaging fluorescence in modifying the surgeon’s conduct during the surgical treatment of advanced gastric cancer - study protocol for an international multicenter prospective study.Front Oncol2022;12:854754 PMCID:PMC8968043

[63] Slooter MD,Cuesta MA,van Berge Henegouwen MI.Fluorescent imaging using indocyanine green during esophagectomy to prevent surgical morbidity: a systematic review and meta-analysis.J Thorac Dis2019;11:S755-65 PMCID:PMC6503266

[64] Peltrini R,Castiglioni S.Intraoperative use of indocyanine green fluorescence imaging in rectal cancer surgery: the state of the art.World J Gastroenterol2021;27:6374-86 PMCID:PMC8517789

[65] Ohi M,Mohri Y.Prevalence of anastomotic leak and the impact of indocyanine green fluorescein imaging for evaluating blood flow in the gastric conduit following esophageal cancer surgery.Esophagus2017;14:351-9 PMCID:PMC5603633

[66] Zehetner J,Alicuben ET.Intraoperative assessment of perfusion of the gastric graft and correlation with anastomotic leaks after esophagectomy.Ann Surg2015;262:74-8 PMCID:PMC4463028

[67] Kondo A,Asano E,Kobara H.Indocyanine green fluorescence imaging during laparoscopic rectal cancer surgery could reduce the incidence of anastomotic leakage: a single institutional retrospective cohort study.World J Surg Oncol2022;20:397 PMCID:PMC9746152

[68] Sherwinter DA,Donkar T.Intra-operative transanal near infrared imaging of colorectal anastomotic perfusion: a feasibility study.Colorectal Dis2013;15:91-6

[69] Huh YJ,Kim TH.Efficacy of assessing intraoperative bowel perfusion with near-infrared camera in laparoscopic gastric cancer surgery.J Laparoendosc Adv Surg Tech A2019;29:476-83

[70] Noma K,Kanaya N.Visualized evaluation of blood flow to the gastric conduit and complications in esophageal reconstruction.J Am Coll Surg2018;226:241-51

[71] Luo RJ,He ZF,Wang YZ.Efficacy of indocyanine green fluorescence angiography in preventing anastomotic leakage after McKeown Minimally invasive esophagectomy.Front Oncol2020;10:619822 PMCID:PMC7821423

[72] Kumagai Y,Sobajima J.Indocyanine green fluorescence angiography of the reconstructed gastric tube during esophagectomy: efficacy of the 90-second rule.Dis Esophagus2018;31:doy052

[73] Mori M,Hirano A.A novel parameter identified using indocyanine green fluorescence angiography may contribute to predicting anastomotic leakage in gastric cancer surgery.World J Surg2020;44:2699-708

[74] Hayakawa S,Ueno S.Impact of the indocyanine green fluorescence method for anastomotic blood flow in robotic distal gastrectomy.Surg Today2022;52:1405-13

[75] Slooter MD,Bloemen PR.Defining indocyanine green fluorescence to assess anastomotic perfusion during gastrointestinal surgery: systematic review.BJS Open2021;5:zraa074 PMCID:PMC8271268

[76] Rawicz-Pruszyński K,Pelc Z.Staging laparoscopy to assess lymph node involvement in advanced gastric cancer (POLA) - study protocol for a single-arm prospective observational multicenter study.PLoS One2023;18:e0285758 PMCID:PMC10198545