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General Thoracic and Cardiovascular Surgery

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01-09-2020 | NSCLC | Review Article

Diagnostic accuracy of sentinel lymph node biopsy using indocyanine green in lung cancer: a systematic review and meta-analysis

Authors: Warren Y. L. Sun, Jerry T. Dang, Aryan Modasi, Awrad Nasralla, Noah J. Switzer, Daniel Birch, Simon R. Turner, Shahzeer Karmali

Published in: General Thoracic and Cardiovascular Surgery | Issue 9/2020

Abstract

Objective

The use of sentinel lymph node biopsy (SLNB) has been gaining popularity with the emergence of indocyanine green (ICG) fluorescence imaging. We aimed to systematically review the literature and perform a meta-analysis on the diagnostic accuracy of SLNB using ICG for lung cancer.

Methods

A comprehensive search of MEDLINE, EMBASE, SCOPUS, Web of Science, and the Cochrane Library using search terms “lung/pulmonary” AND “tumor/carcinoma/cancer/neoplasm/adenocarcinoma/malignancy/squamous/carcinoid” AND “indocyanine green” was completed in June 2018. Articles were selected based on the following inclusion criteria: (1) diagnostic accuracy study design; (2) ICG injected at the tumor site with near-infrared fluorescence imaging identification of sentinel lymph nodes; (3) lymphadenectomy or sampling was performed as the gold standard.

Results

Eight primary studies were included with a total of 366 patients. 43.0% of patients were females and the mean tumor size was 2.3 cm. Sentinel lymph nodes were identified with ICG in 251 patients, yielding a pooled identification rate of 0.83 (0.67–0.94). A meta-analysis of seven studies computed a diagnostic odds ratio, sensitivity, and specificity of 177.6 (45.6–691.1), 0.85 (0.71–0.94), and 1.00 (0.98–1.00), respectively. The summary receiver operator characteristic demonstrated an area under the curve of 0.963 (SE = 0.038) and a Q* of 0.91 (SE = 0.057).

Conclusion

Our review found suboptimal results for the diagnostic accuracy of SLNB using ICG and must be improved before routine clinical use. Further research is required to develop a robust protocol for the use SLNB with ICG for lung cancer.

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Darling GE, Allen MS, Decker PA, Ballman K, Malthaner RA, Inculet RI, Jones DR, McKenna RJ, Landreneau RJ, Rusch VW, Putnam JB Jr. Randomized trial of mediastinal lymph node sampling versus complete lymphadenectomy during pulmonary resection in the patient with N0 or N1 (less than hilar) non-small cell carcinoma: results of the American College of Surgery Oncology Group Z0030 Trial. J Thorac Cardiovasc Surg. 2011;141(3):662–70. https://doi.org/10.1016/j.jtcvs.2010.11.008.CrossRefPubMedPubMedCentral

Gajra A, Newman N, Gamble GP, Kohman LJ, Graziano SL. Effect of number of lymph nodes sampled on outcome in patients with stage I non-small-cell lung cancer. J Clin Oncol. 2003;21(6):1029–34. https://doi.org/10.1200/JCO.2003.07.010.CrossRefPubMed

Lardinois D, De Leyn P, Van Schil P, Porta RR, Waller D, Passlick B, Zielinski M, Lerut T, Weder W. ESTS guidelines for intraoperative lymph node staging in non-small cell lung cancer. Eur J Cardiothorac Surg. 2006;30(5):787–92. https://doi.org/10.1016/j.ejcts.2006.08.008.CrossRefPubMed

Lim E, Baldwin D, Beckles M, Duffy J, Entwisle J, Faivre-Finn C, Kerr K, Macfie A, McGuigan J, Padley S, Popat S, Screaton N, Snee M, Waller D, Warburton C, Win T, British Thoracic S. Society for Cardiothoracic Surgery in Great B, Ireland 2010 Guidelines on the radical management of patients with lung cancer. Thorax. 2019;65(3):1–27. https://doi.org/10.1136/thx.2010.145938.CrossRef

Manser R, Wright G, Hart D, Byrnes G, Campbell DA. Surgery for early stage non-small cell lung cancer. Cochrane Database Syst Rev. 2005;2(1):46–99. https://doi.org/10.1002/14651858.CD004699.pub2.CrossRef

Karamustafaoglu YA, Yoruk Y, Yanik F, Sarikaya A. Sentinel lymph node mapping in patients with operable non-small cell lung cancer. J Thorac Dis. 2013;5(3):317–20. https://doi.org/10.3978/j.issn.2072-1439.2013.06.01.CrossRefPubMedPubMedCentral

Lyman GH, Somerfield MR, Bosserman LD, Perkins CL, Weaver DL, Giuliano AE. Sentinel lymph node biopsy for patients with early-stage breast cancer: american society of clinical oncology clinical practice guideline update. J Clin Oncol. 2017;35(5):561–4. https://doi.org/10.1200/JCO.2016.71.0947.CrossRefPubMed

Morton DL, Wen DR, Wong JH, Economou JS, Cagle LA, Storm FK, Foshag LJ, Cochran AJ. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg. 1992;127(4):392–9.CrossRefPubMed

Caso R, Jones GD, Jones DR. Sentinel lymph node mapping in lung cancer: a step forward? J Thorac Dis. 2018;10(Suppl 26):S3254–S32563256. https://doi.org/10.21037/jtd.2018.08.114.CrossRefPubMedPubMedCentral

10.

Taghizadeh Kermani A, Bagheri R, Tehranian S, Shojaee P, Sadeghi R. Accuracy of sentinel node biopsy in the staging of non-small cell lung carcinomas: systematic review and meta-analysis of the literature. Lung Cancer. 2013;80(1):5–14. https://doi.org/10.1016/j.lungcan.2013.01.001.CrossRefPubMed

11.

Allen MS, Darling GE, Pechet TT, Mitchell JD, Herndon JE, Landreneau RJ, Inculet RI, Jones DR, Meyers BF, Harpole DH, Putnam JB Jr, Rusch VW. Group AZS Morbidity and mortality of major pulmonary resections in patients with early-stage lung cancer: initial results of the randomized, prospective ACOSOG Z0030 trial. Ann Thorac Surg. 2006;81(3):1013–9. https://doi.org/10.1016/j.athoracsur.2005.06.066.CrossRefPubMed

12.

Merritt RE, Hoang CD, Shrager JB. Lymph node evaluation achieved by open lobectomy compared with thoracoscopic lobectomy for N0 lung cancer. Ann Thorac Surg. 2013;96(4):1171–7. https://doi.org/10.1016/j.athoracsur.2013.05.044.CrossRefPubMed

13.

Takeda AH, Watanabe Y, Nagata T, Aoki M, Umehara T, Suzuki S, Kamimura G, Wakida K, Otsuka T, Yokomakura N, Kariatsumari K, Sakasegawa K, Nakamura Y, Sato M. Detection of alternative subpleural lymph flow pathways using indocyanine green fluorescence. Surg Today. 2018;48(6):640–8. https://doi.org/10.1007/s00595-018-1631-1.CrossRefPubMed

14.

Sugi K, Fukuda M, Nakamura H, Kaneda Y. Comparison of three tracers for detecting sentinel lymph nodes in patients with clinical N0 lung cancer. Lung Cancer. 2003;39(1):37–40.CrossRefPubMed

15.

Liptay MJ, D’Amico TA, Nwogu C, Demmy TL, Wang XF, Gu L, Litle VR, Swanson SJ, Kohman LJ. Group B Intraoperative sentinel node mapping with technitium-99 in lung cancer: results of CALGB 140203 multicenter phase II trial. J Thorac Oncol. 2009;4(2):198–202. https://doi.org/10.1097/JTO.0b013e318194a2c3.CrossRefPubMed

16.

Emile SH, Elfeki H, Shalaby M, Sakr A, Sileri P, Laurberg S, Wexner SD. Sensitivity and specificity of indocyanine green near-infrared fluorescence imaging in detection of metastatic lymph nodes in colorectal cancer: systematic review and meta-analysis. J Surg Oncol. 2017;116(6):730–40. https://doi.org/10.1002/jso.24701.CrossRefPubMed

17.

He M, Jiang Z, Wang C, Hao Z, An J, Shen J. Diagnostic value of near-infrared or fluorescent indocyanine green guided sentinel lymph node mapping in gastric cancer: a systematic review and meta-analysis. J Surg Oncol. 2018. https://doi.org/10.1002/jso.25285.CrossRefPubMed

18.

Liberale G, Bohlok A, Bormans A, Bouazza F, Galdon MG, El Nakadi I, Bourgeois P, Donckier V. Indocyanine green fluorescence imaging for sentinel lymph node detection in colorectal cancer: a systematic review. Eur J Surg Oncol. 2018;44(9):1301–6. https://doi.org/10.1016/j.ejso.2018.05.034.CrossRefPubMed

19.

Skubleny D, Dang JT, Skulsky S, Switzer N, Tian C, Shi X, de Gara C, Birch DW, Karmali 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 Endosc. 2018;32(6):2620–31. https://doi.org/10.1007/s00464-018-6100-9.CrossRefPubMed

20.

Digesu CS, Hachey KJ, Gilmore DM, Khullar OV, Tsukada H, Whang B, Chirieac LR, Padera RF, Jaklitsch MT, Colson YL. Long-term outcomes after near-infrared sentinel lymph node mapping in non-small cell lung cancer. J Thorac Cardiovasc Surg. 2018;155(3):1280–91. https://doi.org/10.1016/j.jtcvs.2017.09.150.CrossRefPubMed

21.

Digesu CS, Weiss KD, Colson YL. Near-infrared sentinel lymph node identification in non-small cell lung cancer. JAMA Surg. 2018;153(5):487–8. https://doi.org/10.1001/jamasurg.2017.5928.CrossRefPubMedPubMedCentral

22.

Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, Leeflang MM, Sterne JA, Bossuyt PM. Group Q- QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–36. https://doi.org/10.7326/0003-4819-155-8-201110180-00009.CrossRefPubMed

23.

Glas AS, Lijmer JG, Prins MH, Bonsel GJ, Bossuyt PM. The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol. 2003;56(11):1129–35.CrossRefPubMed

24.

Rosman AS, Korsten MA. Application of summary receiver operating characteristics (sROC) analysis to diagnostic clinical testing. Adv Med Sci. 2007;52:76–82.PubMed

25.

Walter SD. Properties of the summary receiver operating characteristic (SROC) curve for diagnostic test data. Stat Med. 2002;21(9):1237–56. https://doi.org/10.1002/sim.1099.CrossRefPubMed

26.

Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–60. https://doi.org/10.1136/bmj.327.7414.557.CrossRefPubMedPubMedCentral

27.

Akopov A, Papayan G, Chistiakov I, Dvorecky S, Ilyin A. Near-infrared fluorescent identification of lymphatic flow in non-small cell lung cancer. J Thorac Oncol. 2017;12(1):13–85. https://doi.org/10.1016/j.jtho.2016.11.1963.CrossRef

28.

Gilmore DM, Khullar OV, Jaklitsch MT, Chirieac LR, Frangioni JV, Colson YL. Identification of metastatic nodal disease in a phase 1 dose-escalation trial of intraoperative sentinel lymph node mapping in non-small cell lung cancer using near-infrared imaging. J Thorac Cardiovasc Surg. 2013;146(3):562–70. https://doi.org/10.1016/j.jtcvs.2013.04.010.CrossRefPubMedPubMedCentral

29.

Hachey KJ, Digesu CS, Armstrong KW, Gilmore DM, Khullar OV, Whang B, Tsukada H, Colson YL. A novel technique for tumor localization and targeted lymphatic mapping in early-stage lung cancer. J Thorac Cardiovasc Surg. 2017;154(3):1110–8. https://doi.org/10.1016/j.jtcvs.2016.12.058.CrossRefPubMedPubMedCentral

30.

Ichinose S, Usuda J, Maehara S, Ohtani K, Ishizumi T, Ohira T, Kato H, Ikeda N. Sentinel node navigation surgery (SNNS) using indocyanine green (ICG) and near infrared spectroscopy in lung cancer. Philadelphia: Willey; 2009.

31.

Ito N, Fukuta M, Tokushima T, Nakai K, Ohgi S. Sentinel node navigation surgery using indocyanine green in patients with lung cancer. Surg Today. 2004;34(7):581–5. https://doi.org/10.1007/s00595-004-2780-y.CrossRefPubMed

32.

Matsuoka H, Kondo K, Takizawa H, Uyama K, Hiroaki T, Koichiro K, Sakiyama S, Tangoku A. Sentinel lymph nodes detection using indocyanine green in patients with lung cancer. J. Thorac. Oncol. 2009;4:562–3.

33.

Nomori H, Cong Y, Sugimura H. Utility and pitfalls of sentinel node identification using indocyanine green during segmentectomy for cT1N0M0 non-small cell lung cancer. Surg Today. 2016;46(8):908–13. https://doi.org/10.1007/s00595-015-1248-6.CrossRefPubMed

34.

Yamashita S, Tokuishi K, Miyawaki M, Anami K, Moroga T, Takeno S, Chujo M, Yamamoto S, Kawahara K. Sentinel node navigation surgery by thoracoscopic fluorescence imaging system and molecular examination in non-small cell lung cancer. Ann Surg Oncol. 2012;19(3):728–33. https://doi.org/10.1245/s10434-011-2145-x.CrossRefPubMed

35.

Goldstraw P, Chansky K, Crowley J, Rami-Porta R, Asamura H, Eberhardt WE, Nicholson AG, Groome P, Mitchell A, Bolejack V. The IASLC lung cancer staging project: proposals for revision of the tnm stage groupings in the forthcoming (eighth) edition of the tnm classification for lung cancer. J Thorac Oncol. 2016;11(1):39–51. https://doi.org/10.1016/j.jtho.2015.09.009.CrossRefPubMed

36.

Silvestri GA, Gonzalez AV, Jantz MA, Margolis ML, Gould MK, Tanoue LT, Harris LJ, Detterbeck FC. Methods for staging non-small cell lung cancer: diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest. 2013;143(5 Suppl):e211S–e250S250S. https://doi.org/10.1378/chest.12-2355.CrossRefPubMed

37.

Shersher DD, Liptay MJ. Status of sentinel lymph node mapping in non-small cell lung cancer. Cancer J. 2015;21(1):17–20. https://doi.org/10.1097/PPO.0000000000000089.CrossRefPubMed

38.

Imai K, Minamiya Y, Saito H, Nakagawa T, Ito M, Ono T, Motoyama S, Sato Y, Konno H, Ogawa J. Detection of pleural lymph flow using indocyanine green fluorescence imaging in non-small cell lung cancer surgery: a preliminary study. Surg Today. 2013;43(3):249–54. https://doi.org/10.1007/s00595-012-0237-2.CrossRefPubMed

39.

Khullar O, Frangioni JV, Grinstaff M, Colson YL. Image-guided sentinel lymph node mapping and nanotechnology-based nodal treatment in lung cancer using invisible near-infrared fluorescent light. Semin Thorac Cardiovasc Surg. 2009;21(4):309–15. https://doi.org/10.1053/j.semtcvs.2009.11.009.CrossRefPubMedPubMedCentral

40.

Shimkin MB, Connelly RR, Marcus SC, Cutler SJ. Pneumonectomy and lobectomy in bronchogenic carcinoma. A comparison of end results of the overholt and ochsner clinics. J Thorac Cardiovasc Surg. 1962;44:503–19.CrossRefPubMed

Title: Diagnostic accuracy of sentinel lymph node biopsy using indocyanine green in lung cancer: a systematic review and meta-analysis
Authors: Warren Y. L. Sun
Jerry T. Dang
Aryan Modasi
Awrad Nasralla
Noah J. Switzer
Daniel Birch
Simon R. Turner
Shahzeer Karmali
Publication date: 01-09-2020
Publisher: Springer Singapore
Keywords: NSCLC
Lung Cancer
Lung Cancer
NSCLC
Lung Cancer
Published in: General Thoracic and Cardiovascular Surgery / Issue 9/2020
Print ISSN: 1863-6705
Electronic ISSN: 1863-6713
DOI: https://doi.org/10.1007/s11748-020-01400-8

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Diagnostic accuracy of sentinel lymph node biopsy using indocyanine green in lung cancer: a systematic review and meta-analysis

Abstract

Objective

Methods

Results

Conclusion

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Objective

Methods

Results

Conclusion

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