Journal of Gastric Cancer

The Korean Gastric Cancer Association (대한위암학회)
권호 표지
DOI QR코드

DOI QR Code

Recent Advances in Sentinel Node Navigation Surgery for Early Gastric Cancer

  • Eisuke Booka (Department of Surgery, Hamamatsu University School of Medicine) ;
  • Hiroya Takeuchi (Department of Surgery, Hamamatsu University School of Medicine)
  • Received : 2022.12.07
  • Accepted : 2022.12.20
  • Published : 2023.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

Maintaining the postoperative quality of life (QOL) while ensuring curability without overtreatment is important in the treatment of early gastric cancer. Postoperative QOL is anticipated to be maintained through minimally invasive function-preserving gastrectomy in early gastric cancer. The concept of the sentinel lymph node (SN) basin is essential to maintain the curability of early gastric cancer using minimally invasive function-preserving gastrectomy. However, additional resection after surgery is difficult to perform in gastric cancer. Thus, the SN basin theory is important. Recently, a multicenter randomized phase III trial in South Korea (SENORITA trial) proved that laparoscopic sentinel node navigation surgery (LSNNS) for stomach preservation results in better postoperative QOL compared with standard gastrectomy in patients with early gastric cancer. LSNNS contributes to patients' QOL based on the concept that curability is not impaired. A multicenter nonrandomized phase III trial is ongoing in Japan, and oncologic safety is expected to be demonstrated. LSNNS has been established as a treatment option for selected patients with early gastric cancer, and its application will become widespread in the future.

Keywords

Acknowledgement

The authors thank all the patients and medical staff who contributed to this review.

References

  1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;71:209-249.  https://doi.org/10.3322/caac.21660
  2. Japanese Gastric Cancer Association. Japanese gastric cancer treatment guidelines 2018 (5th edition). Gastric Cancer 2021;24:1-21.  https://doi.org/10.1007/s10120-020-01042-y
  3. Kanaji S, Suzuki S, Matsuda Y, Hasegawa H, Yamamoto M, Yamashita K, et al. Recent updates in perioperative chemotherapy and recurrence pattern of gastric cancer. Ann Gastroenterol Surg 2018;2:400-405.  https://doi.org/10.1002/ags3.12199
  4. Morton DL, Thompson JF, Cochran AJ, Mozzillo N, Elashoff R, Essner R, et al. Sentinel-node biopsy or nodal observation in melanoma. N Engl J Med 2006;355:1307-1317.  https://doi.org/10.1056/NEJMoa060992
  5. Kelley MC, Hansen N, McMasters KM. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Am J Surg 2004;188:49-61.  https://doi.org/10.1016/j.amjsurg.2003.10.028
  6. Ryu KW, Eom BW, Nam BH, Lee JH, Kook MC, Choi IJ, et al. 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 2011;104:578-584. https://doi.org/10.1002/jso.21995
  7. Miwa K, Kinami S, Taniguchi K, Fushida S, Fujimura T, Nonomura A. Mapping sentinel nodes in patients with early-stage gastric carcinoma. Br J Surg 2003;90:178-182.  https://doi.org/10.1002/bjs.4031
  8. Kim YW, Min JS, Yoon HM, An JY, Eom BW, Hur H, et al. Laparoscopic sentinel node navigation surgery for stomach preservation in patients with early gastric cancer: a randomized clinical trial. J Clin Oncol 2022;40:2342-2351.  https://doi.org/10.1200/JCO.21.02242
  9. Kitagawa Y, Fujii H, Mukai M, Kubota T, Ando N, Watanabe M, et al. The role of the sentinel lymph node in gastrointestinal cancer. Surg Clin North Am 2000;80:1799-1809.  https://doi.org/10.1016/S0039-6109(05)70262-0
  10. Morton DL, Wen DR, Wong JH, Economou JS, Cagle LA, Storm FK, et al. Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 1992;127:392-399.  https://doi.org/10.1001/archsurg.1992.01420040034005
  11. Hiramatsu Y, Takeuchi H, Goto O, Kikuchi H, Kitagawa Y. Minimally invasive function-preserving gastrectomy with sentinel node biopsy for early gastric cancer. Digestion 2019;99:14-20.  https://doi.org/10.1159/000494407
  12. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 1994;220:391-398.  https://doi.org/10.1097/00000658-199409000-00015
  13. Bilchik AJ, Saha S, Wiese D, Stonecypher JA, Wood TF, Sostrin S, et al. Molecular staging of early colon cancer on the basis of sentinel node analysis: a multicenter phase II trial. J Clin Oncol 2001;19:1128-1136.  https://doi.org/10.1200/jco.2001.19.4.1128
  14. Wang Z, Dong ZY, Chen JQ, Liu JL. Diagnostic value of sentinel lymph node biopsy in gastric cancer: a meta-analysis. Ann Surg Oncol 2012;19:1541-1550.  https://doi.org/10.1245/s10434-011-2124-2
  15. Kitagawa Y, Fujii H, Mukai M, Kubota T, Ando N, Ozawa S, et al. Intraoperative lymphatic mapping and sentinel lymph node sampling in esophageal and gastric cancer. Surg Oncol Clin N Am 2002;11:293-304.  https://doi.org/10.1016/S1055-3207(02)00005-4
  16. Kitagawa Y, Ohgami M, Fujii H, Mukai M, Kubota T, Ando N, et al. Laparoscopic detection of sentinel lymph nodes in gastrointestinal cancer: a novel and minimally invasive approach. Ann Surg Oncol 2001;8 Suppl:86S-89S. 
  17. Kitagawa Y, Fujii H, Mukai M, Kubota T, Otani Y, Kitajima M. Radio-guided sentinel node detection for gastric cancer. Br J Surg 2002;89:604-608.  https://doi.org/10.1046/j.1365-2168.2002.02065.x
  18. Kitagawa Y, Fujii H, Mukai M, Kubo A, Kitajima M. Current status and future prospects of sentinel node navigational surgery for gastrointestinal cancers. Ann Surg Oncol 2004;11 Suppl:242S-244S.  https://doi.org/10.1245/ASO.2004.12.914
  19. Kitagawa Y, Takeuchi H, Takagi Y, Natsugoe S, Terashima M, Murakami N, et al. Sentinel node mapping for gastric cancer: a prospective multicenter trial in Japan. J Clin Oncol 2013;31:3704-3710.  https://doi.org/10.1200/JCO.2013.50.3789
  20. Matsuda S, Irino T, Kawakubo H, Takeuchi H, Kitagawa Y. Current status and challenges in sentinel node navigation surgery for early gastric cancer. Chin J Cancer Res 2021;33:150-158.  https://doi.org/10.21147/j.issn.1000-9604.2021.02.03
  21. Lee JH, Lee HJ, Kong SH, Park DJ, Lee HS, Kim WH, et al. Analysis of the lymphatic stream to predict sentinel nodes in gastric cancer patients. Ann Surg Oncol 2014;21:1090-1098.  https://doi.org/10.1245/s10434-013-3392-9
  22. Kinami S, Fujimura T, Ojima E, Fushida S, Ojima T, Funaki H, et al. PTD classification: proposal for a new classification of gastric cancer location based on physiological lymphatic flow. Int J Clin Oncol 2008;13:320-329.  https://doi.org/10.1007/s10147-007-0755-x
  23. Niihara M, Takeuchi H, Nakahara T, Saikawa Y, Takahashi T, Wada N, et al. Sentinel lymph node mapping for 385 gastric cancer patients. J Surg Res 2016;200:73-81.  https://doi.org/10.1016/j.jss.2015.06.064
  24. Shimada A, Takeuchi H, Kamiya S, Fukuda K, Nakamura R, Takahashi T, et al. Clinical significance of the anterosuperior lymph nodes along the common hepatic artery identified by sentinel node mapping in patients with gastric cancer. Gastric Cancer 2016;19:1088-1094. https://doi.org/10.1007/s10120-015-0563-3
  25. Lee YJ, Jeong SH, Hur H, Han SU, Min JS, An JY, et al. 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) 2015;94:e1894. 
  26. Arigami T, Uenosono Y, Yanagita S, Matsushita D, Arima H, Hirata M, et al. Feasibility of sentinel node navigation surgery after noncurative endoscopic resection for early gastric cancer. J Gastroenterol Hepatol 2013;28:1343-1347.  https://doi.org/10.1111/jgh.12269
  27. Natsugoe S, Arigami T, Uenosono Y, Yanagita S. Novel surgical approach based on the sentinel node concept in patients with early gastric cancer. Ann Gastroenterol Surg 2017;1:180-185.  https://doi.org/10.1002/ags3.12027
  28. Miyashiro I, Hiratsuka M, Sasako M, Sano T, Mizusawa J, Nakamura K, et al. 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 2014;17:316-323.  https://doi.org/10.1007/s10120-013-0285-3
  29. Kim SG, Eom BW, Yoon HM, Kim CG, Kook MC, Kim YW, et al. Recent updates and current issues of sentinel node navigation surgery for early gastric cancer. Chin J Cancer Res 2021;33:142-149.  https://doi.org/10.21147/j.issn.1000-9604.2021.02.02
  30. Park DJ, Kim HH, Park YS, Lee HS, Lee WW, Lee HJ, et al. Simultaneous indocyanine green and (99m)Tcantimony sulfur colloid-guided laparoscopic sentinel basin dissection for gastric cancer. Ann Surg Oncol 2011;18:160-165.  https://doi.org/10.1245/s10434-010-1221-y
  31. Takeuchi H, Kitagawa Y. New sentinel node mapping technologies for early gastric cancer. Ann Surg Oncol 2013;20:522-532.  https://doi.org/10.1245/s10434-012-2602-1
  32. Jimenez IR, Roca M, Vega E, Garcia ML, Benitez A, Bajen M, et al. Particle sizes of colloids to be used in sentinel lymph node radiolocalization. Nucl Med Commun 2008;29:166-172.  https://doi.org/10.1097/MNM.0b013e3282f258d9
  33. Lee JH, Ryu KW, Kim CG, Kim SK, Lee JS, Kook MC, et al. Sentinel node biopsy using dye and isotope double tracers in early gastric cancer. Ann Surg Oncol 2006;13:1168-1174.  https://doi.org/10.1245/s10434-006-9038-4
  34. Nimura H, Narimiya N, Mitsumori N, Yamazaki Y, Yanaga K, Urashima M. Infrared ray electronic endoscopy combined with indocyanine green injection for detection of sentinel nodes of patients with gastric cancer. Br J Surg 2004;91:575-579.  https://doi.org/10.1002/bjs.4470
  35. Takahashi N, Nimura H, Fujita T, Mitsumori N, Shiraishi N, Kitano S, et al. Laparoscopic sentinel node navigation surgery for early gastric cancer: a prospective multicenter trial. Langenbecks Arch Surg 2017;402:27-32.  https://doi.org/10.1007/s00423-016-1540-y
  36. Miyashiro I, Miyoshi N, Hiratsuka M, Kishi K, Yamada T, Ohue M, et al. Detection of sentinel node in gastric cancer surgery by indocyanine green fluorescence imaging: comparison with infrared imaging. Ann Surg Oncol 2008;15:1640-1643.  https://doi.org/10.1245/s10434-008-9872-7
  37. Xiong L, Gazyakan E, Yang W, Engel H, Hunerbein M, Kneser U, et al. Indocyanine green fluorescence-guided sentinel node biopsy: a meta-analysis on detection rate and diagnostic performance. Eur J Surg Oncol 2014;40:843-849.  https://doi.org/10.1016/j.ejso.2014.02.228
  38. Tajima Y, Yamazaki K, Masuda Y, Kato M, Yasuda D, Aoki T, et al. Sentinel node mapping guided by indocyanine green fluorescence imaging in gastric cancer. Ann Surg 2009;249:58-62.  https://doi.org/10.1097/SLA.0b013e3181927267
  39. Tajima Y, Murakami M, Yamazaki K, Masuda Y, Kato M, Sato A, et al. Sentinel node mapping guided by indocyanine green fluorescence imaging during laparoscopic surgery in gastric cancer. Ann Surg Oncol 2010;17:1787-1793.  https://doi.org/10.1245/s10434-010-0944-0
  40. Yano K, Nimura H, Mitsumori N, Takahashi N, Kashiwagi H, Yanaga K. The efficiency of micrometastasis by sentinel node navigation surgery using indocyanine green and infrared ray laparoscopy system for gastric cancer. Gastric Cancer 2012;15:287-291. https://doi.org/10.1007/s10120-011-0105-6
  41. . Tummers QR, Boogerd LS, de Steur WO, Verbeek FP, Boonstra MC, Handgraaf HJ, et al. Near-infrared fluorescence sentinel lymph node detection in gastric cancer: A pilot study. World J Gastroenterol 2016;22:3644-3651.  https://doi.org/10.3748/wjg.v22.i13.3644
  42. Kinami S, Oonishi T, Fujita J, Tomita Y, Funaki H, Fujita H, et al. Optimal settings and accuracy of indocyanine green fluorescence imaging for sentinel node biopsy in early gastric cancer. Oncol Lett 2016;11:4055-4062.  https://doi.org/10.3892/ol.2016.4492
  43. Mehdorn AS, Richter F, Hess K, Beckmann JH, Egberts JH, Linecker M, et al. The Role of ICG in Robot-Assisted Liver Resections. J Clin Med 2022;11:3527. 
  44. Wakabayashi T, Cacciaguerra AB, Abe Y, Bona ED, Nicolini D, Mocchegiani F, et al. Indocyanine green fluorescence navigation in liver surgery: a systematic review on dose and timing of administration. Ann Surg 2022;275:1025-1034.  https://doi.org/10.1097/SLA.0000000000005406
  45. Marino MV, Di Saverio S, Podda M, Gomez Ruiz M, Gomez Fleitas M. The application of indocyanine green fluorescence imaging during robotic liver resection: a case-matched study. World J Surg 2019;43:2595-2606.  https://doi.org/10.1007/s00268-019-05055-2
  46. Park JY, Kook MC, Eom BW, Yoon HM, Kim SJ, Rho JY, et al. 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 2016;25:139-146.  https://doi.org/10.1016/j.suronc.2016.05.004
  47. Wei J, Bu Z. Sentinel lymph node detection for gastric cancer: promise or pitfall? Surg Oncol 2020;33:1-6.  https://doi.org/10.1016/j.suronc.2019.12.005
  48. Uenosono Y, Natsugoe S, Ehi K, Arigami T, Hokita S, Aikou T. Detection of sentinel nodes and micrometastases using radioisotope navigation and immunohistochemistry in patients with gastric cancer. Br J Surg 2005;92:886-889.  https://doi.org/10.1002/bjs.4953
  49. Arigami T, Natsugoe S, Uenosono Y, Mataki Y, Ehi K, Higashi H, et al. Evaluation of sentinel node concept in gastric cancer based on lymph node micrometastasis determined by reverse transcription-polymerase chain reaction. Ann Surg 2006;243:341-347.  https://doi.org/10.1097/01.sla.0000201453.65534.f1
  50. Kumagai K, Yamamoto N, Miyashiro I, Tomita Y, Katai H, Kushima R, et al. Multicenter study evaluating the clinical performance of the OSNA assay for the molecular detection of lymph node metastases in gastric cancer patients. Gastric Cancer 2014;17:273-280.  https://doi.org/10.1007/s10120-013-0271-9
  51. Shimizu Y, Takeuchi H, Sakakura Y, Saikawa Y, Nakahara T, Mukai M, et al. 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 2012;19:469-477.  https://doi.org/10.1245/s10434-011-2122-4
  52. Yaguchi Y, Sugasawa H, Tsujimoto H, Takata H, Nakabayashi K, Ichikura T, et al. One-step nucleic acid amplification (OSNA) for the application of sentinel node concept in gastric cancer. Ann Surg Oncol 2011;18:2289-2296.  https://doi.org/10.1245/s10434-011-1591-9
  53. Shimada A, Takeuchi H, Nishi T, Mayanagi S, Fukuda K, Suda K, et al. Utility of the one-step nucleic acid amplification assay in sentinel node mapping for early gastric cancer patients. Gastric Cancer 2020;23:418-425.  https://doi.org/10.1007/s10120-019-01016-9
  54. Shoji Y, Kumagai K, Kamiya S, Ida S, Nunobe S, Ohashi M, et al. 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 2019;22:873-880.  https://doi.org/10.1007/s10120-018-00919-3
  55. Eom BW, Kim YI, Yoon HM, Cho SJ, Lee JY, Kim CG, et al. Current status and challenges in sentinel node navigation surgery for early gastric cancer. Chin J Cancer Res 2017;29:93-99.  https://doi.org/10.21147/j.issn.1000-9604.2017.02.01
  56. Arroyo-Martinez Q, Han WH, Eom BW, Yoon HM, Kim YI, Cho SJ, et al. The distribution pattern of metastatic lymph nodes after non-curative endoscopic resection in early gastric cancer. J Surg Oncol 2018;118:1257-1263 https://doi.org/10.1002/jso.25279
  57. Mayanagi S, Takeuchi H, Kamiya S, Niihara M, Nakamura R, Takahashi T, et al. Suitability of sentinel node mapping as an index of metastasis in early gastric cancer following endoscopic resection. Ann Surg Oncol 2014;21:2987-2993.  https://doi.org/10.1245/s10434-014-3662-1
  58. Nohara K, Goto O, Takeuchi H, Sasaki M, Maehata T, Yahagi N, et al. Gastric lymphatic flows may change before and after endoscopic submucosal dissection: in vivo porcine survival models. Gastric Cancer 2019;22:723-730.  https://doi.org/10.1007/s10120-018-00920-w
  59. Mayanagi S, Takahashi N, Mitsumori N, Arigami T, Natsugoe S, Yaguchi Y, et al. Sentinel node mapping for post-endoscopic resection gastric cancer: multicenter retrospective cohort study in Japan. Gastric Cancer 2020;23:716-724.  https://doi.org/10.1007/s10120-019-01038-3
  60. Eom BW, Yoon HM, Min JS, Cho I, Park JH, Jung MR, et al. Prospective multicenter feasibility study of laparoscopic sentinel basin dissection after endoscopic submucosal dissection for early gastric cancer: SENORITA 2 trial protocol. J Gastric Cancer 2019;19:157-164.  https://doi.org/10.5230/jgc.2019.19.e12
  61. Aoyama J, Kawakubo H, Goto O, Nakahara T, Mayanagi S, Fukuda K, et al. Potential for local resection with sentinel node basin dissection for early gastric cancer based on the distribution of primary sites. Gastric Cancer 2019;22:386-391.  https://doi.org/10.1007/s10120-018-0865-3
  62. Hiki N, Nunobe S, Kubota T, Jiang X. Function-preserving gastrectomy for early gastric cancer. Ann Surg Oncol 2013;20:2683-2692.  https://doi.org/10.1245/s10434-013-2931-8
  63. Nunobe S, Hiki N, Gotoda T, Murao T, Haruma K, Matsumoto H, et al. Successful application of laparoscopic and endoscopic cooperative surgery (LECS) for a lateral-spreading mucosal gastric cancer. Gastric Cancer 2012;15:338-342.  https://doi.org/10.1007/s10120-012-0146-5
  64. Goto O, Mitsui T, Fujishiro M, Wada I, Shimizu N, Seto Y, et al. New method of endoscopic full-thickness resection: a pilot study of non-exposed endoscopic wall-inversion surgery in an ex vivo porcine model. Gastric Cancer 2011;14:183-187.  https://doi.org/10.1007/s10120-011-0014-8
  65. Goto O, Takeuchi H, Kawakubo H, Sasaki M, Matsuda T, Matsuda S, et al. First case of non-exposed endoscopic wall-inversion surgery with sentinel node basin dissection for early gastric cancer. Gastric Cancer 2015;18:434-439.  https://doi.org/10.1007/s10120-014-0406-7
  66. Kim CG, Yoon HM, Lee JY, Cho SJ, Kook MC, Eom BW, et al. Nonexposure endolaparoscopic fullthickness resection with simple suturing technique. Endoscopy 2015;47:1171-1174.  https://doi.org/10.1055/s-0034-1392271
  67. Eom BW, Kim CG, Kook MC, Yoon HM, Ryu KW, Kim YW, et al. Non-exposure simple suturing endoscopic full-thickness resection with sentinel basin dissection in patients with early gastric cancer: the SENORITA 3 pilot study. J Gastric Cancer 2020;20:245-255.  https://doi.org/10.5230/jgc.2020.20.e22
  68. Kamiya S, Takeuchi H, Fukuda K, Kawakubo H, Takahashi N, Mitsumori N, et al. A multicenter nonrandomized phase III study of sentinel node navigation surgery for early gastric cancer. Jpn J Clin Oncol 2021;51:305-309.  https://doi.org/10.1093/jjco/hyaa179
  69. Park JY, Kim YW, Ryu KW, Nam BH, Lee YJ, Jeong SH, et al. 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 2016;16:340. 
  70. An JY, Min JS, Hur H, Lee YJ, Cho GS, Park YK, et al. Laparoscopic sentinel node navigation surgery versus laparoscopic gastrectomy with lymph node dissection for early gastric cancer: short-term outcomes of a multicentre randomized controlled trial (SENORITA). Br J Surg 2020;107:1429-1439.  https://doi.org/10.1002/bjs.11655
  71. Hiramatsu Y, Kikuchi H, Takeuchi H. Function-preserving gastrectomy for early gastric cancer. Cancers (Basel) 2021;13:6223.