Abstract
Background
Sentinel lymph node biopsy (SLNB) plays an essential role in the evaluation of lymph node (LN) metastasis status and the extent of LN dissection in gastric cancer. The aim of our study was to perform a systematic review and meta-analysis for corresponding identification rate and sensitivity of different SLNB techniques.
Methods
Systematic search using PubMed, Embase, and Cochrane library databases was conducted for studies on SLNB in patients with gastric cancer. Studies were stratified according to the sentinel lymph node (SLN) biopsy technique: blue dye (BD), radiocolloid tracer (RI), indocyanine green (ICG), a combination of radiocolloid with blue dye (RI + BD), and a combination of radiocolloid with ICG (RI + ICG). A random-effect model was used to pool the identification rate, sensitivity, and accuracy.
Results
A total of 54 eligible studies (3767 patients) was included. The pooled identification rates of SLNB using BD, RI, ICG, RI + BD, RI + ICG were 95% (95%CI: 92–97%), 95% (95%CI: 93–97%), 99% (95%CI: 97–99%), 97% (95%CI: 96–98%), and 95% (95%CI: 87–99%), respectively. The pooled sensitivities were 82% (95%CI: 77–86%), 87% (95%CI: 81–92%), 90% (95%CI: 82–95%), 89% (95%CI: 84–93%), and 88% (95%CI: 79–94%), respectively. The pooled accuracies were 94% (95%CI: 91–96%), 95% (95%CI: 92–97%), 98% (95%CI: 95–99%), 97% (95%CI: 95–99%), and 98% (95%CI: 95–99%), respectively.
Conclusions
The current meta-analysis provides reliable evidence that favors the use of ICG and dual tracer method (RI + BD/ICG) for the identification of the SLN. Considering the high costs and potential biohazard of using radioactive substances in dual tracer method, performing SLNB with ICG is the technique of choice for experienced surgeons.
Similar content being viewed by others
References
Bray F, Ferlay J, Soerjomataram I et al (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424
Straver ME, Meijnen P, van Tienhoven G et al (2010) Sentinel node identification rate and nodal involvement in the EORTC 10981–22023 AMAROS trial. Ann Surg Oncol 17:1854–1861
Miyashiro I, Kishi K, Yano M et al (2011) Laparoscopic detection of sentinel node in gastric cancer surgery by indocyanine green fluorescence imaging. Surg Endosc 25:1672–1676
Yoshida M, Kubota K, Kuroda J et al (2012) Indocyanine green injection for detecting sentinel nodes using color fluorescence camera in the laparoscopy-assisted gastrectomy. J Gastroenterol Hepatol 27(Suppl 3):29–33
Takeuchi H, Kitagawa Y (2013) New sentinel node mapping technologies for early gastric cancer. Ann Surg Oncol 20:522–532
Park DJ, Kim HH, Park YS et al (2011) Simultaneous indocyanine green and (99 m)Tc-antimony sulfur colloid-guided laparoscopic sentinel basin dissection for gastric cancer. Ann Surg Oncol 18:160–165
Saikawa Y, Otani Y, Kitagawa Y et al (2006) Interim results of sentinel node biopsy during laparoscopic gastrectomy: possible role in function-preserving surgery for early cancer. World J Surg 30:1962–1968. https://doi.org/10.1007/s00268-006-0142-1
Takahashi N, Nimura H, Fujita T et al (2017) Laparoscopic sentinel node navigation surgery for early gastric cancer: a prospective multicenter trial. Langenbecks Arch Surg 402:27–32
Skubleny D, Dang JT, Skulsky S et al (2018) 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 Endosc 32:2620–2631
Jalaly NY, Valizadeh N, Azizi S et al (2014) Sentinel lymph node mapping and biopsy using radioactive tracer in gastric cancer. ANZ J Surg 84:454–458
Kitagawa Y, Fujii H, Mukai M et al (2002) Radio-guided sentinel node detection for gastric cancer. Br J Surg 89:604–608
Shoji Y, Kumagai K, Kamiya S et al (2019) Prospective feasibility study for single-tracer sentinel node mapping by ICG (indocyanine green) fluorescence and OSNA (one-step nucleic acid amplification) assay in laparoscopic gastric cancer surgery. Gastric Cancer 22:873–880
Bostick P, Essner R, Glass E et al (1999) Comparison of blue dye and probe-assisted intraoperative lymphatic mapping in melanoma to identify sentinel nodes in 100 lymphatic basins. Arch Surg 134:43–49
Giuliano AE, Jones RC, Brennan M et al (1997) Sentinel lymphadenectomy in breast cancer. J Clin Oncol 15:2345–2350
Takahashi N, Nimura H, Fujita T et al (2016) Quantitative assessment of visual estimation of the infrared indocyanine green imaging of lymph nodes retrieved at sentinel node navigation surgery for gastric cancer. BMC Surg 16:35
Tajima Y, Yamazaki K, Masuda Y et al (2009) Sentinel node mapping guided by indocyanine green fluorescence imaging in gastric cancer. Ann Surg 249:58–62
Morgan JW, Ji L, Friedman G et al (2015) The role of the cancer center when using lymph node count as a quality measure for gastric cancer surgery. JAMA Surg 150:37–43
Whiting PF, Rutjes AW, Westwood ME et al (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536
DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188
Bara T Jr, Gurzu S, Jung I et al (2019) Sentinel node biospy using intravital blue dye: an useful technique for identification of skip metastases in gastric cancer. Medicine (Baltimore) 98:e14951
Isozaki H, Matsumoto S, Murakami S (2019) Survival outcomes after sentinel node navigation surgery for early gastric cancer. Ann Gastroenterol Surg 3:552–560
Dong LF, Wang LB, Shen JG et al (2012) Sentinel lymph node biopsy predicts lymph node metastasis in early gastric cancer: a retrospective analysis. Dig Surg 29:124–129
Toth D, Kincses Z, Plosz J et al (2011) Value of sentinel lymph node mapping using a blue dye-only method in gastric cancer: a single-center experience from North-East Hungary. Gastric Cancer 14:360–364
Cozzaglio L, Bottura R, Di Rocco M et al (2011) Sentinel lymph node biopsy in gastric cancer: possible applications and limits. Eur J Surg Oncol 37:55–59
Rabin I, Chikman B, Lavy R et al (2010) The accuracy of sentinel node mapping according to T stage in patients with gastric cancer. Gastric Cancer 13:30–35
Becher RD, Shen P, Stewart JH et al (2009) Sentinel lymph node mapping for gastric adenocarcinoma. Am Surg 75:710–714
Orsenigo E, Tomajer V, Di Palo S et al (2008) Sentinel node mapping during laparoscopic distal gastrectomy for gastric cancer. Surg Endosc 22:118–121
Rino Y, Takanashi Y, Harada H et al (2006) Technique and assessment of sentinel lymph node biopsy usefulness in laparoscopy-assisted distal gastrectomy. Surg Endosc 20:1887–1891
Rabin I, Chikman B, Halpern Z et al (2006) Sentinel node mapping for gastric cancer. Isr Med Assoc J 8:40–43
Miyake K, Seshimo A, Kameoka S (2006) Assessment of lymph node micrometastasis in early gastric cancer in relation to sentinel nodes. Gastric Cancer 9:197–202
Ishizaki M, Kurita A, Kubo Y et al (2006) Evaluation of sentinel node identification with isosulfan blue in gastric cancer. Eur J Surg Oncol 32:191–196
Lee JH, Ryu KW, Kim CG et al (2005) Comparative study of the subserosal versus submucosal dye injection method for sentinel node biopsy in gastric cancer. Eur J Surg Oncol 31:965–968
Gretschel S, Bembenek A, Ulmer C et al (2005) Prediction of gastric cancer lymph node status by sentinel lymph node biopsy and the Maruyama computer model. Eur J Surg Oncol 31:393–400
Fu XB, Hu X (2005) Localization and pathological examination of sentinel lymph node during operation in gastric cancer. Zhonghua Wei Chang Wai Ke Za Zhi 8:29–31
Song X, Wang L, Chen W et al (2004) Lymphatic mapping and sentinel node biopsy in gastric cancer. Am J Surg 187:270–273
Osaka H, Yashiro M, Sawada T et al (2004) Is a lymph node detected by the dye-guided method a true sentinel node in gastric cancer? Clin Cancer Res 10:6912–6918
Ryu KW, Lee JH, Kim HS et al (2003) Prediction of lymph nodes metastasis by sentinel node biopsy in gastric cancer. Eur J Surg Oncol 29:895–899
Miwa K, Kinami S, Taniguchi K et al (2003) Mapping sentinel nodes in patients with early-stage gastric carcinoma. Br J Surg 90:178–182
Shida A, Mitsumori N, Fujioka S et al (2018) Sentinel node navigation surgery for early gastric cancer: analysis of factors which affect direction of lymphatic drainage. World J Surg 42:766–772. https://doi.org/10.1007/s00268-017-4226-x
Tummers QR, Boogerd LS, de Steur WO et al (2016) Near-infrared fluorescence sentinel lymph node detection in gastric cancer: a pilot study. World J Gastroenterol 22:3644–3651
Kinami S, Oonishi T, Fujita J et al (2016) Optimal settings and accuracy of indocyanine green fluorescence imaging for sentinel node biopsy in early gastric cancer. Oncol Lett 11:4055–4062
Tajima Y, Murakami M, Yamazaki K et al (2010) Sentinel node mapping guided by indocyanine green fluorescence imaging during laparoscopic surgery in gastric cancer. Ann Surg Oncol 17:1787–1793
Kelder W, Nimura H, Takahashi N et al (2010) 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 Oncol 36:552–558
Ishikawa K, Yasuda K, Shiromizu A et al (2007) Laparoscopic sentinel node navigation achieved by infrared ray electronic endoscopy system in patients with gastric cancer. Surg Endosc 21:1131–1134
Su XH, Chen Q, Sun L et al (2010) Location of sentinel lymph node in gastric cancer: A modified, painless and noninvasive approach. Chin J Cancer Res 22:55–61
Mochiki E, Kuwano H, Kamiyama Y et al (2006) Sentinel lymph node mapping with technetium-99m colloidal rhenium sulfide in patients with gastric carcinoma. Am J Surg 191:465–469
Zulfikaroglu B, Koc M, Ozmen MM et al (2005) Intraoperative lymphatic mapping and sentinel lymph node biopsy using radioactive tracer in gastric cancer. Surgery 138:899–904
Uenosono Y, Natsugoe S, Ehi K et al (2005) Detection of sentinel nodes and micrometastases using radioisotope navigation and immunohistochemistry in patients with gastric cancer. Br J Surg 92:886–889
Kim MC, Kim HH, Jung GJ et al (2004) Lymphatic mapping and sentinel node biopsy using 99mTc tin colloid in gastric cancer. Ann Surg 239:383–387
Gretschel S, Bembenek A, Ulmer C et al (2003) Lymphatic mapping and sentinel lymph node biopsy in gastric cancer. Chirurg 74:132–138
Mueller CL, Lisbona R, Sorial R et al (2019) Sentinel lymph node sampling for early gastric cancer-preliminary results of a north american prospective study. J Gastrointest Surg 23:1113–1121
Ohi M, Toiyama Y, Omura Y et al (2019) Possibility of limited gastrectomy for early gastric cancer located in the upper third of the stomach, based on the distribution of sentinel node basins. Surg Today 49:529–535
Niihara M, Takeuchi H, Nakahara T et al (2016) Sentinel lymph node mapping for 385 gastric cancer patients. J Surg Res 200:73–81
Kitagawa Y, Takeuchi H, Takagi Y et al (2013) Sentinel node mapping for gastric cancer: a prospective multicenter trial in Japan. J Clin Oncol 31:3704–3710
Gretschel S, Bembenek A, Hunerbein M et al (2007) Efficacy of different technical procedures for sentinel lymph node biopsy in gastric cancer staging. Ann Surg Oncol 14:2028–2035
Mura G, Vagliasindi A, Framarini M et al (2006) The sentinel node biopsy in early gastric cancer: a preliminary study. Langenbecks Arch Surg 391:113–117
Lee JH, Ryu KW, Kim CG et al (2006) Sentinel node biopsy using dye and isotope double tracers in early gastric cancer. Ann Surg Oncol 13:1168–1174
Tonouchi H, Mohri Y, Tanaka K et al (2005) Laparoscopic lymphatic mapping and sentinel node biopsies for early-stage gastric cancer: the cause of false negativity. World J Surg 29:418–421
Cheng LY, Chen XD, Zhang YX et al (2005) Clinical significance of sentinel lymph node detection by combining the dye-directed and radioguided methods in gastric cancer. Zhonghua Wai Ke Za Zhi 43:569–572
Karube T, Ochiai T, Shimada H et al (2004) Detection of sentinel lymph nodes in gastric cancers based on immunohistochemical analysis of micrometastases. J Surg Oncol 87:32–38
Tonouchi H, Mohri Y, Tanaka K et al (2003) Lymphatic mapping and sentinel node biopsy during laparoscopic gastrectomy for early cancer. Dig Surg 20:421–427
Hayashi H, Ochiai T, Mori M et al (2003) Sentinel lymph node mapping for gastric cancer using a dual procedure with dye- and gamma probe-guided techniques. J Am Coll Surg 196:68–74
Park DJ, Park YS, Son SY et al (2018) Long-term oncologic outcomes of laparoscopic sentinel node navigation surgery in early gastric cancer: a single-center, single-arm, phase II trial. Ann Surg Oncol 25:2357–2365
Kamiya S, Takeuchi H, Nakahara T et al (2016) Auxiliary diagnosis of lymph node metastasis in early gastric cancer using quantitative evaluation of sentinel node radioactivity. Gastric Cancer 19:1080–1087
Lee YJ, Jeong SH, Hur H et al (2015) Prospective multicenter feasibility study of laparoscopic sentinel basin dissection for organ preserving surgery in gastric cancer: quality control study for surgical standardization prior to phase III trial. Medicine (Baltimore) 94:e1894
Yaguchi Y, Ichikura T, Ono S et al (2008) 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 27:79
Lee YJ, Ha WS, Park ST et al (2008) 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 A 18:357–363
Lee JH, Ryu KW, Kook MC et al (2008) Feasibility of laparoscopic sentinel basin dissection for limited resection in early gastric cancer. J Surg Oncol 98:331–335
Kusano M, Tajima Y, Yamazaki K et al (2008) Sentinel node mapping guided by indocyanine green fluorescence imaging: a new method for sentinel node navigation surgery in gastrointestinal cancer. Dig Surg 25:103–108
Kitai T, Inomoto T, Miwa M et al (2005) Fluorescence navigation with indocyanine green for detecting sentinel lymph nodes in breast cancer. Breast Cancer 12:211–215
Miyashiro I, Miyoshi N, Hiratsuka M et al (2008) Detection of sentinel node in gastric cancer surgery by indocyanine green fluorescence imaging: comparison with infrared imaging. Ann Surg Oncol 15:1640–1643
Miyashiro I, Hiratsuka M, Sasako M et al (2014) 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 Cancer 17:316–323
Funding
This research was supported by the Natural Science Foundation of Fujian Province (Grant No. 2018J01377).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
268_2020_5900_MOESM5_ESM.tif
Deeks' funnel plot asymmetry tests for assessing potential publication bias (P value < 0.1 was considered statistically significant). (TIF 575kb)
Rights and permissions
About this article
Cite this article
Huang, Y., Pan, M. & Chen, B. A Systematic Review and Meta-Analysis of Sentinel Lymph Node Biopsy in Gastric Cancer, an Optimization of Imaging Protocol for Tracer Mapping. World J Surg 45, 1126–1134 (2021). https://doi.org/10.1007/s00268-020-05900-9
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00268-020-05900-9