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A Systematic Review and Meta-Analysis of Sentinel Lymph Node Biopsy in Gastric Cancer, an Optimization of Imaging Protocol for Tracer Mapping

World Journal of Surgery volume 45, pages 1126–1134 (2021)Cite this article

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.

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References

  1. 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

    Article  Google Scholar 

  2. 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

    PubMed  PubMed Central  Google Scholar 

  3. 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

    PubMed  Google Scholar 

  4. 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

    CAS  PubMed  Google Scholar 

  5. Takeuchi H, Kitagawa Y (2013) New sentinel node mapping technologies for early gastric cancer. Ann Surg Oncol 20:522–532

    PubMed  Google Scholar 

  6. 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

    PubMed  Google Scholar 

  7. 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

    Article  PubMed  Google Scholar 

  8. 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

    PubMed  Google Scholar 

  9. 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

    PubMed  Google Scholar 

  10. 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

    PubMed  Google Scholar 

  11. Kitagawa Y, Fujii H, Mukai M et al (2002) Radio-guided sentinel node detection for gastric cancer. Br J Surg 89:604–608

    CAS  PubMed  Google Scholar 

  12. 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

    PubMed  Google Scholar 

  13. 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

    CAS  PubMed  Google Scholar 

  14. Giuliano AE, Jones RC, Brennan M et al (1997) Sentinel lymphadenectomy in breast cancer. J Clin Oncol 15:2345–2350

    CAS  PubMed  Google Scholar 

  15. 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

    PubMed  PubMed Central  Google Scholar 

  16. 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

    PubMed  Google Scholar 

  17. 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

    PubMed  Google Scholar 

  18. 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

    PubMed  Google Scholar 

  19. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 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

    CAS  Google Scholar 

  21. Isozaki H, Matsumoto S, Murakami S (2019) Survival outcomes after sentinel node navigation surgery for early gastric cancer. Ann Gastroenterol Surg 3:552–560

    PubMed  PubMed Central  Google Scholar 

  22. 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

    CAS  PubMed  Google Scholar 

  23. 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

    PubMed  Google Scholar 

  24. 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

    CAS  PubMed  Google Scholar 

  25. 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

    PubMed  Google Scholar 

  26. Becher RD, Shen P, Stewart JH et al (2009) Sentinel lymph node mapping for gastric adenocarcinoma. Am Surg 75:710–714

    PubMed  Google Scholar 

  27. 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

    CAS  PubMed  Google Scholar 

  28. 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

    CAS  PubMed  Google Scholar 

  29. Rabin I, Chikman B, Halpern Z et al (2006) Sentinel node mapping for gastric cancer. Isr Med Assoc J 8:40–43

    PubMed  Google Scholar 

  30. 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

    PubMed  Google Scholar 

  31. 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

    CAS  PubMed  Google Scholar 

  32. 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

    CAS  PubMed  Google Scholar 

  33. 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

    CAS  PubMed  Google Scholar 

  34. 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

    PubMed  Google Scholar 

  35. Song X, Wang L, Chen W et al (2004) Lymphatic mapping and sentinel node biopsy in gastric cancer. Am J Surg 187:270–273

    PubMed  Google Scholar 

  36. 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

    PubMed  Google Scholar 

  37. 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

    CAS  PubMed  Google Scholar 

  38. 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

    CAS  PubMed  Google Scholar 

  39. 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

    Article  PubMed  Google Scholar 

  40. 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

    PubMed  PubMed Central  Google Scholar 

  41. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  42. 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

    PubMed  Google Scholar 

  43. 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

    CAS  PubMed  Google Scholar 

  44. 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

    CAS  PubMed  Google Scholar 

  45. 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

    Google Scholar 

  46. 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

    PubMed  Google Scholar 

  47. 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

    PubMed  Google Scholar 

  48. 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

    CAS  PubMed  Google Scholar 

  49. 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

    PubMed  PubMed Central  Google Scholar 

  50. Gretschel S, Bembenek A, Ulmer C et al (2003) Lymphatic mapping and sentinel lymph node biopsy in gastric cancer. Chirurg 74:132–138

    CAS  PubMed  Google Scholar 

  51. 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

    PubMed  Google Scholar 

  52. 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

    PubMed  Google Scholar 

  53. Niihara M, Takeuchi H, Nakahara T et al (2016) Sentinel lymph node mapping for 385 gastric cancer patients. J Surg Res 200:73–81

    PubMed  Google Scholar 

  54. 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

    PubMed  Google Scholar 

  55. 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

    PubMed  Google Scholar 

  56. 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

    PubMed  Google Scholar 

  57. 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

    PubMed  Google Scholar 

  58. 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

    PubMed  Google Scholar 

  59. 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

    PubMed  Google Scholar 

  60. 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

    PubMed  Google Scholar 

  61. 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

    PubMed  Google Scholar 

  62. 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

    PubMed  Google Scholar 

  63. 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

    PubMed  Google Scholar 

  64. 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

    CAS  PubMed  Google Scholar 

  65. 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

    Google Scholar 

  66. 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

    PubMed  PubMed Central  Google Scholar 

  67. 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

    PubMed  Google Scholar 

  68. 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

    PubMed  Google Scholar 

  69. 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

    PubMed  Google Scholar 

  70. 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

    PubMed  Google Scholar 

  71. 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

    PubMed  Google Scholar 

  72. 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

    PubMed  Google Scholar 

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Funding

This research was supported by the Natural Science Foundation of Fujian Province (Grant No. 2018J01377).

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  1. Yuqiang Huang and Mengting Pan contributed equally to this work.

Affiliations

  1. Department of Clinical Medicine, Fujian Medical University, Fuzhou, 350122, China

    Yuqiang Huang & Bo Chen

  2. Department of Gastrointestinal Surgery, Xiamen Cancer Center, The First Affiliated Hospital of Xiamen University, 55 Zhenhai Road, Xiamen, 361003, China

    Yuqiang Huang, Mengting Pan & Bo Chen

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  1. Yuqiang Huang
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Correspondence to Bo Chen.

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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

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