Skip to main content
Top
Published in: Surgical Endoscopy 6/2018

01-06-2018 | Review

Diagnostic evaluation of sentinel lymph node biopsy using indocyanine green and infrared or fluorescent imaging in gastric cancer: a systematic review and meta-analysis

Authors: Daniel Skubleny, Jerry T. Dang, Samuel Skulsky, Noah Switzer, Chunhong Tian, Xinzhe Shi, Christopher de Gara, Daniel W. Birch, Shahzeer Karmali

Published in: Surgical Endoscopy | Issue 6/2018

Login to get access

Abstract

Background

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.

Methods

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.

Results

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%).

Conclusions

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.
Literature
1.
go back to reference Ferro A, Peleteiro B, Malvezzi M, Bosetti C, Bertuccio P, Levi F, Negri E, La Vecchia C, Lunet N (2014) Worldwide trends in gastric cancer mortality (1980–2011), with predictions to 2015, and incidence by subtype. Eur J Cancer 50:1330–1344CrossRefPubMed Ferro A, Peleteiro B, Malvezzi M, Bosetti C, Bertuccio P, Levi F, Negri E, La Vecchia C, Lunet N (2014) Worldwide trends in gastric cancer mortality (1980–2011), with predictions to 2015, and incidence by subtype. Eur J Cancer 50:1330–1344CrossRefPubMed
2.
go back to reference Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359-386CrossRef Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359-386CrossRef
3.
go back to reference 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 79:1522–1530CrossRefPubMedPubMedCentral 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 79:1522–1530CrossRefPubMedPubMedCentral
4.
go back to reference Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ (2010) Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol 11:439–449CrossRefPubMed Songun I, Putter H, Kranenbarg EM, Sasako M, van de Velde CJ (2010) Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol 11:439–449CrossRefPubMed
5.
go back to reference Wu CW, Hsiung CA, Lo SS, Hsieh MC, Chen JH, Li AF, Lui WY, Whang-Peng J (2006) Nodal dissection for patients with gastric cancer: a randomised controlled trial. Lancet Oncol 7:309–315CrossRefPubMed Wu CW, Hsiung CA, Lo SS, Hsieh MC, Chen JH, Li AF, Lui WY, Whang-Peng J (2006) Nodal dissection for patients with gastric cancer: a randomised controlled trial. Lancet Oncol 7:309–315CrossRefPubMed
6.
go back to reference Smith DD, Schwarz RR, Schwarz RE (2005) Impact of total lymph node count on staging and survival after gastrectomy for gastric cancer: data from a large US-population database. J Clin Oncol 23:7114–7124CrossRefPubMed Smith DD, Schwarz RR, Schwarz RE (2005) Impact of total lymph node count on staging and survival after gastrectomy for gastric cancer: data from a large US-population database. J Clin Oncol 23:7114–7124CrossRefPubMed
7.
go back to reference 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 221:291–299CrossRefPubMedPubMedCentral 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 221:291–299CrossRefPubMedPubMedCentral
8.
go back to reference 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 274CrossRef 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 274CrossRef
9.
go back to reference Cooperman AM (1981) Postgastrectomy syndromes. Surg Annu 13:139–161PubMed Cooperman AM (1981) Postgastrectomy syndromes. Surg Annu 13:139–161PubMed
10.
11.
go back to reference 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 31:3704–3710CrossRefPubMed 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 31:3704–3710CrossRefPubMed
12.
go back to reference Mitsumori N, Nimura H, Takahashi N, Kawamura M, Aoki H, Shida A, Omura N, Yanaga K (2014) Sentinel lymph node navigation surgery for early stage gastric cancer. World J Gastroenterol 20:5685–5693CrossRefPubMedPubMedCentral Mitsumori N, Nimura H, Takahashi N, Kawamura M, Aoki H, Shida A, Omura N, Yanaga K (2014) Sentinel lymph node navigation surgery for early stage gastric cancer. World J Gastroenterol 20:5685–5693CrossRefPubMedPubMedCentral
13.
go back to reference Wang Z, Dong ZY, Chen JQ, Liu JL (2012) Diagnostic value of sentinel lymph node biopsy in gastric cancer: a meta-analysis. Ann Surg Oncol 19:1541–1550CrossRefPubMed Wang Z, Dong ZY, Chen JQ, Liu JL (2012) Diagnostic value of sentinel lymph node biopsy in gastric cancer: a meta-analysis. Ann Surg Oncol 19:1541–1550CrossRefPubMed
14.
go back to reference Fujimura T, Fushida S, Tsukada T, Kinoshita J, Oyama K, Miyashita T, Takamura H, Kinami S, Ohta T (2015) A new stage of sentinel node navigation surgery in early gastric cancer. Gastric Cancer 18:210–217CrossRefPubMed Fujimura T, Fushida S, Tsukada T, Kinoshita J, Oyama K, Miyashita T, Takamura H, Kinami S, Ohta T (2015) A new stage of sentinel node navigation surgery in early gastric cancer. Gastric Cancer 18:210–217CrossRefPubMed
15.
16.
go back to reference 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 17:316–323CrossRefPubMed 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 17:316–323CrossRefPubMed
17.
go back to reference Xiong L, Gazyakan E, Yang W, Engel H, Hunerbein M, Kneser U, Hirche C (2014) Indocyanine green fluorescence-guided sentinel node biopsy: a meta-analysis on detection rate and diagnostic performance. Eur J Surg Oncol 40:843–849CrossRefPubMed Xiong L, Gazyakan E, Yang W, Engel H, Hunerbein M, Kneser U, Hirche C (2014) Indocyanine green fluorescence-guided sentinel node biopsy: a meta-analysis on detection rate and diagnostic performance. Eur J Surg Oncol 40:843–849CrossRefPubMed
18.
go back to reference Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536CrossRefPubMed Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536CrossRefPubMed
19.
go back to reference Glas AS, Lijmer JG, Prins MH, Bonsel GJ, Bossuyt PM (2003) The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 56:1129–1135CrossRefPubMed Glas AS, Lijmer JG, Prins MH, Bonsel GJ, Bossuyt PM (2003) The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 56:1129–1135CrossRefPubMed
20.
go back to reference Rosman AS, Korsten MA (2007) Application of summary receiver operating characteristics (sROC) analysis to diagnostic clinical testing. Adv Med Sci 52:76–82PubMed Rosman AS, Korsten MA (2007) Application of summary receiver operating characteristics (sROC) analysis to diagnostic clinical testing. Adv Med Sci 52:76–82PubMed
21.
go back to reference Walter SD (2002) Properties of the summary receiver operating characteristic (SROC) curve for diagnostic test data. Stat Med 21:1237–1256CrossRefPubMed Walter SD (2002) Properties of the summary receiver operating characteristic (SROC) curve for diagnostic test data. Stat Med 21:1237–1256CrossRefPubMed
22.
go back to reference 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/ 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/​
24.
go back to reference Kusano M, Tajima Y, Yamazaki K, Kato M, Watanabe M, Miwa M (2008) Sentinel node mapping guided by indocyanine green fluorescence imaging: a new method for sentinel node navigation surgery in gastrointestinal cancer. Dig Surg 25:103–108CrossRefPubMed Kusano M, Tajima Y, Yamazaki K, Kato M, Watanabe M, Miwa M (2008) Sentinel node mapping guided by indocyanine green fluorescence imaging: a new method for sentinel node navigation surgery in gastrointestinal cancer. Dig Surg 25:103–108CrossRefPubMed
25.
go back to reference Tajima Y, Murakami M, Yamazaki K, Masuda Y, Kato M, Sato A, Goto S, Otsuka K, Kato T, Kusano M (2010) Sentinel node mapping guided by indocyanine green fluorescence imaging during laparoscopic surgery in gastric cancer. Ann Surg Oncol 17:1787–1793CrossRefPubMed Tajima Y, Murakami M, Yamazaki K, Masuda Y, Kato M, Sato A, Goto S, Otsuka K, Kato T, Kusano M (2010) Sentinel node mapping guided by indocyanine green fluorescence imaging during laparoscopic surgery in gastric cancer. Ann Surg Oncol 17:1787–1793CrossRefPubMed
26.
go back to reference 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 26:276–281CrossRefPubMed 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 26:276–281CrossRefPubMed
27.
go back to reference Ohdaira H, Nimura H, Takahashi N, Mitsumori N, Kashiwagi H, Narimiya N, Yanaga K (2009) The possibility of performing a limited resection and a lymphadenectomy for proximal gastric carcinoma based on sentinel node navigation. Surg Today 39:1026–1031CrossRefPubMed Ohdaira H, Nimura H, Takahashi N, Mitsumori N, Kashiwagi H, Narimiya N, Yanaga K (2009) The possibility of performing a limited resection and a lymphadenectomy for proximal gastric carcinoma based on sentinel node navigation. Surg Today 39:1026–1031CrossRefPubMed
28.
go back to reference Yano K, Nimura H, Mitsumori N, Takahashi N, Kashiwagi H, Yanaga K (2012) The efficiency of micrometastasis by sentinel node navigation surgery using indocyanine green and infrared ray laparoscopy system for gastric cancer. Gastric Cancer 15:287–291CrossRefPubMed Yano K, Nimura H, Mitsumori N, Takahashi N, Kashiwagi H, Yanaga K (2012) The efficiency of micrometastasis by sentinel node navigation surgery using indocyanine green and infrared ray laparoscopy system for gastric cancer. Gastric Cancer 15:287–291CrossRefPubMed
29.
go back to reference Kinami S, Oonishi T, Fujita J, Tomita Y, Funaki H, Fujita H, Nakano Y, Ueda N, Kosaka T (2016) Optimal settings and accuracy of indocyanine green fluorescence imaging for sentinel node biopsy in early gastric cancer. Oncol Lett 11:4055–4062CrossRefPubMedPubMedCentral Kinami S, Oonishi T, Fujita J, Tomita Y, Funaki H, Fujita H, Nakano Y, Ueda N, Kosaka T (2016) Optimal settings and accuracy of indocyanine green fluorescence imaging for sentinel node biopsy in early gastric cancer. Oncol Lett 11:4055–4062CrossRefPubMedPubMedCentral
30.
go back to reference Takahashi N, Nimura H, Fujita T, Mitsumori N, Shiraishi N, Kitano S, Satodate H, Yanaga K (2017) Laparoscopic sentinel node navigation surgery for early gastric cancer: a prospective multicenter trial. Langenbeck’s Arch Surg 402:27–32CrossRef Takahashi N, Nimura H, Fujita T, Mitsumori N, Shiraishi N, Kitano S, Satodate H, Yanaga K (2017) Laparoscopic sentinel node navigation surgery for early gastric cancer: a prospective multicenter trial. Langenbeck’s Arch Surg 402:27–32CrossRef
31.
go back to reference 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 22:3644–3651CrossRefPubMedPubMedCentral 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 22:3644–3651CrossRefPubMedPubMedCentral
32.
go back to reference Ishikawa K, Yasuda K, Shiromizu A, Etoh T, Shiraishi N, Kitano S (2007) Laparoscopic sentinel node navigation achieved by infrared ray electronic endoscopy system in patients with gastric cancer. Surg Endosc 21:1131–1134CrossRefPubMed Ishikawa K, Yasuda K, Shiromizu A, Etoh T, Shiraishi N, Kitano S (2007) Laparoscopic sentinel node navigation achieved by infrared ray electronic endoscopy system in patients with gastric cancer. Surg Endosc 21:1131–1134CrossRefPubMed
33.
go back to reference Kelder W, Nimura H, Takahashi N, Mitsumori N, van Dam GM, Yanaga K (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 36:552–558CrossRefPubMed Kelder W, Nimura H, Takahashi N, Mitsumori N, van Dam GM, Yanaga K (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 36:552–558CrossRefPubMed
34.
go back to reference Ryu KW, Eom BW, Nam BH, Lee JH, Kook MC, Choi IJ, Kim YW (2011) 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 Oncol 104:578–584CrossRefPubMed Ryu KW, Eom BW, Nam BH, Lee JH, Kook MC, Choi IJ, Kim YW (2011) 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 Oncol 104:578–584CrossRefPubMed
35.
go back to reference 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 39:1286–1290 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 39:1286–1290
36.
go back to reference Miyashiro I, Miyoshi N, Hiratsuka M, Kishi K, Yamada T, Ohue M, Ohigashi H, Yano M, Ishikawa O, Imaoka S (2008) Detection of sentinel node in gastric cancer surgery by indocyanine green fluorescence imaging: comparison with infrared imaging. Ann Surg Oncol 15:1640–1643CrossRefPubMed Miyashiro I, Miyoshi N, Hiratsuka M, Kishi K, Yamada T, Ohue M, Ohigashi H, Yano M, Ishikawa O, Imaoka S (2008) Detection of sentinel node in gastric cancer surgery by indocyanine green fluorescence imaging: comparison with infrared imaging. Ann Surg Oncol 15:1640–1643CrossRefPubMed
37.
go back to reference Nimura H, Narimiya N, Mitsumori N, Yamazaki Y, Yanaga K, Urashima M (2004) Infrared ray electronic endoscopy combined with indocyanine green injection for detection of sentinel nodes of patients with gastric cancer. Br J Surg 91:575–579CrossRefPubMed Nimura H, Narimiya N, Mitsumori N, Yamazaki Y, Yanaga K, Urashima M (2004) Infrared ray electronic endoscopy combined with indocyanine green injection for detection of sentinel nodes of patients with gastric cancer. Br J Surg 91:575–579CrossRefPubMed
38.
go back to reference Cahill RA, Ris F, Mortensen NJ (2011) Near-infrared laparoscopy for real-time intra-operative arterial and lymphatic perfusion imaging. Colorectal Dis 7:12–17CrossRef Cahill RA, Ris F, Mortensen NJ (2011) Near-infrared laparoscopy for real-time intra-operative arterial and lymphatic perfusion imaging. Colorectal Dis 7:12–17CrossRef
39.
go back to reference Sasako M, McCulloch P, Kinoshita T, Maruyama K (1995) New method to evaluate the therapeutic value of lymph node dissection for gastric cancer. Br J Surg 82:346–351CrossRefPubMed Sasako M, McCulloch P, Kinoshita T, Maruyama K (1995) New method to evaluate the therapeutic value of lymph node dissection for gastric cancer. Br J Surg 82:346–351CrossRefPubMed
40.
go back to reference Lee SE, Lee JH, Ryu KW, Cho SJ, Lee JY, Kim CG, Choi IJ, Kook MC, Nam BH, Park SR, Lee JS, Kim YW (2009) Sentinel node mapping and skip metastases in patients with early gastric cancer. Ann Surg Oncol 16:603–608CrossRefPubMed Lee SE, Lee JH, Ryu KW, Cho SJ, Lee JY, Kim CG, Choi IJ, Kook MC, Nam BH, Park SR, Lee JS, Kim YW (2009) Sentinel node mapping and skip metastases in patients with early gastric cancer. Ann Surg Oncol 16:603–608CrossRefPubMed
41.
go back to reference Tajima Y, Yamazaki K, Masuda Y, Kato M, Yasuda D, Aoki T, Kato T, Murakami M, Miwa M, Kusano M (2009) Sentinel node mapping guided by indocyanine green fluorescence imaging in gastric cancer. Ann Surg 249:58–62CrossRefPubMed Tajima Y, Yamazaki K, Masuda Y, Kato M, Yasuda D, Aoki T, Kato T, Murakami M, Miwa M, Kusano M (2009) Sentinel node mapping guided by indocyanine green fluorescence imaging in gastric cancer. Ann Surg 249:58–62CrossRefPubMed
42.
go back to reference (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14:101–112 (2011) Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 14:101–112
43.
go back to reference 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 243:341–347CrossRefPubMedPubMedCentral 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 243:341–347CrossRefPubMedPubMedCentral
44.
go back to reference 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 19:469–477CrossRefPubMed 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 19:469–477CrossRefPubMed
45.
go back to reference 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:e1894CrossRefPubMedPubMedCentral 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:e1894CrossRefPubMedPubMedCentral
46.
go back to reference 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 18:2289–2296CrossRefPubMed 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 18:2289–2296CrossRefPubMed
47.
go back to reference 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 27:7 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 27:7
48.
go back to reference 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 77:205–211CrossRefPubMed 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 77:205–211CrossRefPubMed
49.
go back to reference 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 25:139–146CrossRefPubMed 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 25:139–146CrossRefPubMed
50.
go back to reference Tani T, Sonoda H, Tani M (2016) Sentinel lymph node navigation surgery for gastric cancer: Does it really benefit the patient? World J Gastroenterol 22:2894–2899CrossRefPubMedPubMedCentral Tani T, Sonoda H, Tani M (2016) Sentinel lymph node navigation surgery for gastric cancer: Does it really benefit the patient? World J Gastroenterol 22:2894–2899CrossRefPubMedPubMedCentral
52.
go back to reference 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 16:340CrossRefPubMedPubMedCentral 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 16:340CrossRefPubMedPubMedCentral
Metadata
Title
Diagnostic evaluation of sentinel lymph node biopsy using indocyanine green and infrared or fluorescent imaging in gastric cancer: a systematic review and meta-analysis
Authors
Daniel Skubleny
Jerry T. Dang
Samuel Skulsky
Noah Switzer
Chunhong Tian
Xinzhe Shi
Christopher de Gara
Daniel W. Birch
Shahzeer Karmali
Publication date
01-06-2018
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 6/2018
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-018-6100-9

Other articles of this Issue 6/2018

Surgical Endoscopy 6/2018 Go to the issue