Diagnostic evaluation of sentinel lymph node biopsy using indocyanine green and infrared or fluorescent imaging in gastric cancer: a systematic review and meta-analysis
Sentinel node navigation surgery (SNNS) for gastric cancer using infrared visualization of indocyanine green (ICG) is intriguing because it may limit operative morbidity. We are the first to systematically review and perform meta-analysis on the diagnostic utility of ICG and infrared electronic endoscopy (IREE) or near infrared fluorescent imaging (NIFI) for SNNS exclusively in gastric cancer.
A search of electronic databases MEDLINE, EMBASE, SCOPUS, Web of Science, and the Cochrane Library using search terms “gastric/stomach” AND “tumor/carcinoma/cancer/neoplasm/adenocarcinoma/malignancy” AND “indocyanine green” was completed in May 2017. Articles were selected by two independent reviewers based on the following major inclusion criteria: (1) diagnostic accuracy study design; (2) indocyanine green was injected at tumor site; (3) IREE or NIFI was used for intraoperative visualization. 327 titles or abstracts were screened. The quality of included studies was assessed using the Quality Assessment of Diagnostic Accuracy Studies-2.
Ten full text studies were selected. 643 patients were identified with the majority of patients possessing T1 tumors (79.8%). Pooled identification rate, diagnostic odds ratio, sensitivity, and specificity were 0.99 (0.97–1.0), 380.0 (68.71–2101), 0.87 (0.80–0.93), and 1.00 (0.99–1.00), respectively. The summary receiver operator characteristic for ICG + IREE/NIFI demonstrated a test accuracy of 98.3%. Subgroup analysis found improved test performance for studies with low-risk QUADAS-2 scores, studies published after 2010 and submucosal ICG injection. IREE had improved diagnostic odds ratio, sensitivity, and identification rate compared to NIFI. Heterogeneity among studies ranged from low (I2 < 25%) to high (I2 > 75%).
We found encouraging results regarding the accuracy, diagnostic odds ratio, and specificity of the test. The sensitivity was not optimal but may be improved by a strict protocol to augment the technique. Given the number and heterogeneity of studies, our results must be viewed with caution.
KeywordsGastric Sentinel Node Indocyanine green Infrared
Compliance with ethical standards
Ms. Xinzhe Shi, Chunghong Tian, Drs Daniel Skubleny, Jerry T. Dang, Samuel Skulsky, Noah Switzer, Christopher de Gara, Daniel W. Birch, and Shahzeer Karmali have no conflicts of interest or financial ties to disclose.
- 3.Cuschieri A, Weeden S, Fielding J, Bancewicz J, Craven J, Joypaul V, Sydes M, Fayers P (1999) Patient survival after D1 and D2 resections for gastric cancer: long-term results of the MRC randomized surgical trial. surgical co-operative group. Br J Cancer 79:1522–1530CrossRefPubMedPubMedCentralGoogle Scholar
- 7.Gholami S, Janson L, Worhunsky DJ, Tran TB, Squires MH, 3rd, Jin LX, Spolverato G, Votanopoulos KI, Schmidt C, Weber SM, Bloomston M, Cho CS, Levine EA, Fields RC, Pawlik TM, Maithel SK, Efron B, Norton JA, Poultsides GA (2015) Number of lymph nodes removed and survival after gastric cancer resection: an analysis from the US gastric cancer collaborative. J Am Coll Surg 221:291–299CrossRefPubMedPubMedCentralGoogle Scholar
- 8.Roviello F, Rossi S, Marrelli D, Pedrazzani C, Corso G, Vindigni C, Morgagni P, Saragoni L, de Manzoni G, Tomezzoli A (2006) Number of lymph node metastases and its prognostic significance in early gastric cancer: a multicenter Italian study. J Surg Oncol 94:275–280; discussion 274CrossRefGoogle Scholar
- 11.Kitagawa Y, Takeuchi H, Takagi Y, Natsugoe S, Terashima M, Murakami N, Fujimura T, Tsujimoto H, Hayashi H, Yoshimizu N, Takagane A, Mohri Y, Nabeshima K, Uenosono Y, Kinami S, Sakamoto J, Morita S, Aikou T, Miwa K, Kitajima M (2013) Sentinel node mapping for gastric cancer: a prospective multicenter trial in Japan. J Clin Oncol 31:3704–3710CrossRefPubMedGoogle Scholar
- 16.Miyashiro I, Hiratsuka M, Sasako M, Sano T, Mizusawa J, Nakamura K, Nashimoto A, Tsuburaya A, Fukushima N (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 17:316–323CrossRefPubMedGoogle Scholar
- 22.Bossuyt PDC, Deeks J, Hyde C, Leeflang M, Scholten R (2013) Chapter 11:Interpreting results and drawing conclusions. In: Deeks JJ, Bossuyt PM, Gatsonis C (eds), Cochrane handbook for systematic reviews of diagnostic test accuracy version 0.9. The cochrane collaboration. http://srdta.cochrane.org/
- 26.Ohdaira H, Nimura H, Fujita T, Mitsumori N, Takahashi N, Kashiwagi H, Narimiya N, Yanaga K (2009) Tailoring treatment for early gastric cancer after endoscopic resection using sentinel node navigation with infrared ray electronic endoscopy combined with indocyanine green injection. Dig Surg 26:276–281CrossRefPubMedGoogle Scholar
- 31.Tummers QR, Boogerd LS, de Steur WO, Verbeek FP, Boonstra MC, Handgraaf HJ, Frangioni JV, van de Velde CJ, Hartgrink HH, Vahrmeijer AL (2016) Near-infrared fluorescence sentinel lymph node detection in gastric cancer: a pilot study. World J Gastroenterol 22:3644–3651CrossRefPubMedPubMedCentralGoogle Scholar
- 35.Yoneya S, Saito T, Komatsu Y, Koyama I, Takahashi K, Duvoll-Young J (1998) Binding properties of indocyanine green in human blood. Investig Ophthalmol Visual Sci 39:1286–1290Google Scholar
- 42.(2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14:101–112Google Scholar
- 43.Arigami T, Natsugoe S, Uenosono Y, Mataki Y, Ehi K, Higashi H, Arima H, Yanagida S, Ishigami S, Hokita S, Aikou T (2006) Evaluation of sentinel node concept in gastric cancer based on lymph node micrometastasis determined by reverse transcription-polymerase chain reaction. Ann Surg 243:341–347CrossRefPubMedPubMedCentralGoogle Scholar
- 44.Shimizu Y, Takeuchi H, Sakakura Y, Saikawa Y, Nakahara T, Mukai M, Kitajima M, Kitagawa Y (2012) Molecular detection of sentinel node micrometastases in patients with clinical N0 gastric carcinoma with real-time multiplex reverse transcription-polymerase chain reaction assay. Ann Surg Oncol 19:469–477CrossRefPubMedGoogle Scholar
- 45.Lee YJ, Jeong SH, Hur H, Han SU, Min JS, An JY, Hyung WJ, Cho GS, Jeong GA, Jeong O, Park YK, Jung MR, Kim YW, Yoon HM, Eom BW, Park JY, Ryu KW (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 94:e1894CrossRefPubMedPubMedCentralGoogle Scholar
- 46.Yaguchi Y, Sugasawa H, Tsujimoto H, Takata H, Nakabayashi K, Ichikura T, Ono S, Hiraki S, Sakamoto N, Horio T, Kumano I, Otomo Y, Mochizuki H, Yamamoto J, Hase K (2011) One-step nucleic acid amplification (OSNA) for the application of sentinel node concept in gastric cancer. Ann Surg Oncol 18:2289–2296CrossRefPubMedGoogle Scholar
- 47.Ishii K, Kinami S, Funaki K, Fujita H, Ninomiya I, Fushida S, Fujimura T, Nishimura G, Kayahara M (2008) Detection of sentinel and non-sentinel lymph node micrometastases by complete serial sectioning and immunohistochemical analysis for gastric cancer. J Exp Clin Cancer Res 27:7Google Scholar
- 48.Yanagita S, Natsugoe S, Uenosono Y, Arigami T, Funasako Y, Hirata M, Kozono T, Ehi K, Arima H, Green G, Wang Y, Aikou T (2009) The utility of rapid diagnosis of lymph node metastasis in gastric cancer using a multiplex real-time reverse transcription polymerase chain reaction assay. Oncology 77:205–211CrossRefPubMedGoogle Scholar
- 49.Park JY, Kook M-C, Eom BW, Yoon HM, Kim SJ, Rho JY, Kim S-K, Kim Y-I, Cho S-J, Lee JY, Kim CG, Choi IJ, Kim Y-W, Ryu KW (2016) Practical intraoperative pathologic evaluation of sentinel lymph nodes during sentinel node navigation surgery in gastric cancer patients – Proposal of the pathologic protocol for the upcoming SENORITA trial. Surg Oncol 25:139–146CrossRefPubMedGoogle Scholar
- 52.Park JY, Kim YW, Ryu KW, Nam BH, Lee YJ, Jeong SH, Park JH, Hur H, Han SU, Min JS, An JY, Hyung WJ, Cho GS, Jeong GA, Jeong O, Park YK, Jung MR, Yoon HM, Eom BW (2016) 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 Cancer 16:340CrossRefPubMedPubMedCentralGoogle Scholar