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Surgical Endoscopy
Published in: Surgical Endoscopy 3/2020

01-03-2020 | Metastasis | Review Article

Performance of Indocyanine green for sentinel lymph node mapping and lymph node metastasis in colorectal cancer: a diagnostic test accuracy meta-analysis

Authors: E. Villegas-Tovar, J. Jimenez-Lillo, V. Jimenez-Valerio, A. Diaz-Giron-Gidi, R. Faes-Petersen, A. Otero-Piñeiro, F. B. De Lacy, R. J. Martinez-Portilla, A. M. Lacy

Published in: Surgical Endoscopy | Issue 3/2020

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Abstract

Background

Indocyanine green has been widely employed as a secure and easy technique for sentinel lymph node mapping in different types of cancer. Nonetheless, the usage of Indocyanine green has not been fully implemented due to the heterogeneous results found in published studies. Thus, the objective of this meta-analysis is to evaluate the overall performance of Indocyanine green for sentinel lymph node mapping and node metastasis in patients undergoing colorectal cancer surgery.

Methods

An extensive systematic search was performed to identify relevant studies in English and Spanish with no time limit restrictions. For the meta-analysis, a hierarchical summary receiver operating characteristic curve (HSROCs) was constructed, and quantitative data synthesis was performed using random effects models. Specificity, sensitivity, positive, and negative likelihood ratios were obtained from the corresponding HSROC. Between-study heterogeneity was visually evaluated using Galbraith plot, and publication bias was quantified using Deeks’ method.

Results

A total of 11 studies were included for analysis. The pooled detection rate for sentinel lymph node mapping was 91% (80–98%). Covariates significantly influencing the pooled detection rate were having colon cancer (estimate: 1.3001; 1.114 to 1.486; p < 0.001) and the usage of a laparoscopic approach (estimate: 1.3495; 1.1029 to 1.5961; p < 0.001). The performance of Indocyanine green for the detection of metastatic lymph nodes yielded an area under the roc curve of 66.5%, sensitivity of 64.3% (51–76%), and specificity of 65% (36–85%).

Conclusions

Indocyanine green for the detection of sentinel lymph node mapping demonstrates better accuracy when used in colonic cancer and by a laparoscopic approach. Nevertheless, its overall performance for the detection of lymph node metastasis is poor.
Appendix
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Literature
1.
Saha S, Sehgal R, Patel M, Doan K, Dan A, Bilchik A, Beutler T, Wiese D, Bassily N, Yee C (2006) A multicenter trial of sentinel lymph node mapping in colorectal cancer: prognostic implications for nodal staging and recurrence. Am J Surg 191:305–310PubMedCrossRef
2.
Saha S, Bilchik A, Wiese D, Espinosa M, Badin J, Ganatra BK, Desai D, Kaushal S, Singh T, Arora M (2001) Ultrastaging of colorectal cancer by sentinel lymph node mapping technique—a multicenter trial. Ann Surg Oncol 8:94S–98SPubMed
3.
van der Pas MH, Meijer S, Hoekstra OS, Riphagen II, de Vet HC, Knol DL, van Grieken NC, Meijerink WJ (2011) Sentinel-lymph-node procedure in colon and rectal cancer: a systematic review and meta-analysis. Lancet Oncol 12:540–550PubMedCrossRef
4.
Baxter NN, Virnig DJ, Rothenberger DA, Morris AM, Jessurun J, Virnig BA (2005) Lymph node evaluation in colorectal cancer patients: a population-based study. J Natl Cancer Inst 97:219–225PubMedCrossRef
5.
Stoffels I, von der Stuck H, Boy C, Poppel T, Korber N, Weindorf M, Dissemond J, Schadendorf D, Klode J (2012) Indocyanine green fluorescence-guided sentinel lymph node biopsy in dermato-oncology. J Dtsch Dermatol Ges 10:51–57PubMed
6.
Namikawa K, Yamazaki N (2011) Sentinel lymph node biopsy guided by indocyanine green fluorescence for cutaneous melanoma. Eur J Dermatol 21:184–190PubMed
7.
Murawa D, Hirche C, Dresel S, Hunerbein M (2009) Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence. Br J Surg 96:1289–1294PubMedCrossRef
8.
Jung SY, Kim SK, Kim SW, Kwon Y, Lee ES, Kang HS, Ko KL, Shin KH, Lee KS, Park IH, Ro J, Jeong HJ, Joo J, Kang SH, Lee S (2014) Comparison of sentinel lymph node biopsy guided by the multimodal method of indocyanine green fluorescence, radioisotope, and blue dye versus the radioisotope method in breast cancer: a randomized controlled trial. Ann Surg Oncol 21:1254–1259PubMedCrossRef
9.
He K, Chi C, Kou D, Huang W, Wu J, Wang Y, He L, Ye J, Mao Y, Zhang GJ, Wang J, Tian J (2016) Comparison between the indocyanine green fluorescence and blue dye methods for sentinel lymph node biopsy using novel fluorescence image-guided resection equipment in different types of hospitals. Transl Res 178:74–80PubMedCrossRef
10.
Chiu CC (2010) Sentinel lymph node biopsy in breast cancer guided by indocyanine green fluorescence (Br J Surg 2009; 96: 1289–1294). Br J Surg 97:455; Author Reply 455–456
11.
Hirche C, Murawa D, Mohr Z, Kneif S, Hunerbein M (2010) ICG fluorescence-guided sentinel node biopsy for axillary nodal staging in breast cancer. Breast Cancer Res Treat 121:373–378PubMedCrossRef
12.
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 91:575–579PubMedCrossRef
13.
Chen SL, Bilchik AJ (2006) More extensive nodal dissection improves survival for stages I to III of colon cancer: a population-based study. Ann Surg 244:602–610PubMedPubMedCentral
14.
Le Voyer TE, Sigurdson ER, Hanlon AL, Mayer RJ, Macdonald JS, Catalano PJ, Haller DG (2003) Colon cancer survival is associated with increasing number of lymph nodes analyzed: a secondary survey of intergroup trial INT-0089. J Clin Oncol 21:2912–2919PubMedCrossRef
15.
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 40:843–849PubMedCrossRef
16.
Sotiriadis A, Papatheodorou SI, Martins WP (2016) Synthesizing Evidence from Diagnostic Accuracy TEsts: the SEDATE guideline. Ultrasound Obstet Gynecol 47:386–395PubMedCrossRef
17.
Fleming PS, Seehra J, Polychronopoulou A, Fedorowicz Z, Pandis N (2013) A PRISMA assessment of the reporting quality of systematic reviews in orthodontics. Angle Orthod 83:158–163PubMedCrossRef
18.
Harbord RM, Deeks JJ, Egger M, Whiting P, Sterne JA (2007) A unification of models for meta-analysis of diagnostic accuracy studies. Biostatistics 8:239–251PubMedCrossRef
19.
Reitsma JB, Glas AS, Rutjes AW, Scholten RJ, Bossuyt PM, Zwinderman AH (2005) Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol 58:982–990PubMedCrossRef
20.
Rutter CM, Gatsonis CA (2001) A hierarchical regression approach to meta-analysis of diagnostic test accuracy evaluations. Stat Med 20:2865–2884PubMedCrossRef
21.
Macaskill P (2004) Empirical Bayes estimates generated in a hierarchical summary ROC analysis agreed closely with those of a full Bayesian analysis. J Clin Epidemiol 57:925–932PubMedCrossRef
22.
Chu H, Cole SR (2006) Bivariate meta-analysis of sensitivity and specificity with sparse data: a generalized linear mixed model approach. J Clin Epidemiol 59:1331–1332; Author Reply 1332–1333PubMedCrossRef
23.
24.
van Enst WA, Ochodo E, Scholten RJ, Hooft L, Leeflang MM (2014) Investigation of publication bias in meta-analyses of diagnostic test accuracy: a meta-epidemiological study. BMC Med Res Methodol 14:70PubMedPubMedCentralCrossRef
25.
Deeks JJ, Macaskill P, Irwig L (2005) The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol 58:882–893PubMedCrossRef
26.
27.
Harbord RM (2008) Metandi: Stata module for meta-analysis of diagnostic accuracy. Statistical Software Components from Boston College Department of Economics Boston College
28.
Andersen HS, Bennedsen ALB, Burgdorf SK, Eriksen JR, Eiholm S, Toxvaerd A, Riis LB, Rosenberg J, Gogenur I (2017) In vivo and ex vivo sentinel node mapping does not identify the same lymph nodes in colon cancer. Int J Colorectal Dis 32:983–990PubMedCrossRef
29.
Cahill RA, Anderson M, Wang LM, Lindsey I, Cunningham C, Mortensen NJ (2012) Near-infrared (NIR) laparoscopy for intraoperative lymphatic road-mapping and sentinel node identification during definitive surgical resection of early-stage colorectal neoplasia. Surg Endosc 26:197–204PubMedCrossRef
30.
Currie AC, Brigic A, Thomas-Gibson S, Suzuki N, Moorghen M, Jenkins JT, Faiz OD, Kennedy RH (2017) A pilot study to assess near infrared laparoscopy with indocyanine green (ICG) for intraoperative sentinel lymph node mapping in early colon cancer. Eur J Surg Oncol 43:2044–2051PubMedCrossRef
31.
Hirche C, Mohr Z, Kneif S, Doniga S, Murawa D, Strik M, Hunerbein M (2012) Ultrastaging of colon cancer by sentinel node biopsy using fluorescence navigation with indocyanine green. Int J Colorectal Dis 27:319–324PubMedCrossRef
32.
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 25:103–108PubMedCrossRef
33.
Liberale G, Galdon MG, Moreau M, Vankerckhove S, El Nakadi I, Larsimont D, Donckier V, Bourgeois P (2016) Ex vivo detection of tumoral lymph nodes of colorectal origin with fluorescence imaging after intraoperative intravenous injection of indocyanine green. J Surg Oncol 114:348–353PubMedCrossRef
34.
Liberale G, Vankerckhove S, Galdon MG, Larsimont D, Ahmed B, Bouazza F, Moreau M, El Nakadi I, Donckier V, Bourgeois P, R&D Group for the Clinical Application of Fluorescence Imaging at the Jules Bordet Institute (2016) Sentinel lymph node detection by blue dye versus indocyanine green fluorescence imaging in colon cancer. Anticancer Res 36:4853–4858PubMedCrossRef
35.
Noura S, Ohue M, Seki Y, Tanaka K, Motoori M, Kishi K, Miyashiro I, Ohigashi H, Yano M, Ishikawa O, Miyamoto Y (2010) Feasibility of a lateral region sentinel node biopsy of lower rectal cancer guided by indocyanine green using a near-infrared camera system. Ann Surg Oncol 17:144–151PubMedCrossRef
36.
Noura S, Ohue M, Seki Y, Yamamoto T, Idota A, Fujii J, Yamasaki T, Nakajima H, Murata K, Kameyama M, Yamada T, Miyashiro I, Ohigashi H, Yano M, Ishikawa O, Imaoka S (2008) Evaluation of the lateral sentinel node by indocyanine green for rectal cancer based on micrometastasis determined by reverse transcriptase-polymerase chain reaction. Oncol Rep 20:745–750PubMed
37.
Watanabe J, Ota M, Suwa Y, Ishibe A, Masui H, Nagahori K (2016) Real-time indocyanine green fluorescence imaging-guided complete mesocolic excision in laparoscopic flexural colon cancer surgery. Dis Colon Rectum 59:701–705PubMedCrossRef
38.
Weixler B, Rickenbacher A, Raptis DA, Viehl CT, Guller U, Rueff J, Zettl A, Zuber M (2017) Sentinel lymph node mapping with isosulfan blue or indocyanine green in colon cancer shows comparable results and identifies patients with decreased survival: a Prospective Single-Center Trial. World J Surg 41:2378–2386PubMedCrossRef
39.
Arezzo A, Arolfo S, Mistrangelo M, Mussa B, Cassoni P, Morino M (2014) Transrectal sentinel lymph node biopsy for early rectal cancer during transanal endoscopic microsurgery. Minim Invasive Ther Allied Technol 23:17–20PubMedCrossRef
40.
Lan YT, Huang KH, Chen PH, Liu CA, Lo SS, Wu CW, Shyr YM, Fang WL (2017) A pilot study of lymph node mapping with indocyanine green in robotic gastrectomy for gastric cancer. SAGE Open Med 5:2050312117727444PubMedPubMedCentralCrossRef
41.
Hirche C, Dresel S, Krempien R, Hunerbein M (2010) Sentinel node biopsy by indocyanine green retention fluorescence detection for inguinal lymph node staging of anal cancer: preliminary experience. Ann Surg Oncol 17:2357–2362PubMedCrossRef
42.
Boni L, David G, Mangano A, Dionigi G, Rausei S, Spampatti S, Cassinotti E, Fingerhut A (2015) Clinical applications of indocyanine green (ICG) enhanced fluorescence in laparoscopic surgery. Surg Endosc 29:2046–2055PubMedCrossRef
43.
Liberale G, Vankerckhove S, Galdon MG, Donckier V, Larsimont D, Bourgeois P (2015) Fluorescence imaging after intraoperative intravenous injection of indocyanine green for detection of lymph node metastases in colorectal cancer. Eur J Surg Oncol 41:1256–1260PubMedCrossRef
44.
Tamura K, Hotta T, Yokoyama S, Matsuda K, Iwamoto H, Yamaue H (2017) Using indocyanine green fluorescent imaging to successfully resect metachronous regional lymph node recurrence of rectosigmoid cancer. Asian J Endosc Surg 11(1):47–49PubMedCrossRef
45.
Keller DS, Ishizawa T, Cohen R, Chand M (2017) Indocyanine green fluorescence imaging in colorectal surgery: overview, applications, and future directions. Lancet Gastroenterol Hepatol 2:757–766PubMedCrossRef
46.
Yeung TM, Wang LM, Colling R, Kraus R, Cahill R, Hompes R, Mortensen NJ (2018) Intraoperative identification and analysis of lymph nodes at laparoscopic colorectal cancer surgery using fluorescence imaging combined with rapid OSNA pathological assessment. Surg Endosc 32:1073–1076PubMedCrossRef
47.
Nishigori N, Koyama F, Nakagawa T, Nakamura S, Ueda T, Inoue T, Kawasaki K, Obara S, Nakamoto T, Fujii H, Nakajima Y (2016) Visualization of lymph/blood flow in laparoscopic colorectal cancer surgery by ICG Fluorescence Imaging (Lap-IGFI). Ann Surg Oncol 23(Suppl 2):S266–S274PubMedCrossRef
48.
Nagata K, Endo S, Hidaka E, Tanaka J, Kudo SE, Shiokawa A (2006) Laparoscopic sentinel node mapping for colorectal cancer using infrared ray laparoscopy. Anticancer Res 26:2307–2311PubMed
49.
Miyoshi N, Ohue M, Noura S, Yano M, Sasaki Y, Kishi K, Yamada T, Miyashiro I, Ohigashi H, Iishi H, Ishikawa O, Imaoka S (2009) Surgical usefulness of indocyanine green as an alternative to India ink for endoscopic marking. Surg Endosc 23:347–351PubMedCrossRef
50.
Handgraaf HJ, Boogerd LS, Verbeek FP, Tummers QR, Hardwick JC, Baeten CI, Frangioni JV, van de Velde CJ, Vahrmeijer AL (2016) Intraoperative fluorescence imaging to localize tumors and sentinel lymph nodes in rectal cancer. Minim Invasive Ther Allied Technol 25:48–53PubMedCrossRef
51.
Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM, QUADAS-2 Group (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536PubMedCrossRef
Metadata
Title
Performance of Indocyanine green for sentinel lymph node mapping and lymph node metastasis in colorectal cancer: a diagnostic test accuracy meta-analysis
Authors
E. Villegas-Tovar
J. Jimenez-Lillo
V. Jimenez-Valerio
A. Diaz-Giron-Gidi
R. Faes-Petersen
A. Otero-Piñeiro
F. B. De Lacy
R. J. Martinez-Portilla
A. M. Lacy
Publication date
01-03-2020
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 3/2020
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-019-07274-z

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