Multi-tracer sentinel node biopsy for patients with breast cancer after neoadjuvant chemotherapy

Main Article Content

Yuko Takao Yuriko Katagiri Rie Sugihara Shumtarou Matsushima Hidetaka Watanabe Nobutaka Iwakuma Miki Yamaguchi Fumitaka Fujita Uhi Toh

Abstract

Background: For post-neoadjuvant chemotherapy patients with breast cancer, sentinel lymph node biopsy (SLNB) was recommended using the dual-tracer mapping technique (radioisotope plus blue dye) or placing a biopsy clip into the positive node at diagnosis and identifying it at the time of surgery due to SLN identification rates were lower and false negative rates were greater for patients with local advanced BC than those of patients with early-stage BC in the absence of NAC. Our previous clinical trial has indicated that the real-time ICG fluorescence (RT-ICG) imaging technique could improve the diagnostic sensitivity and detection accuracy for SLNB.


Methods: The SLNs was detected by conventional procedures of blue-dye (Indigo carmine) plus 99mTc radioisotope (dual-tracer) and combined with concurrent RT-ICG technique. The positivity of each single SN by each single tracer (blue dye, ICG, or radioisotope alone) was counted and identified, respectively. 51 enrolled cN1patients after NAC are required to undergo SNB followed by completion axillary lymph node dissection (CND). The identification rate and false negative rate of each single tracer and their summation (triple tracer) were calculated by comparing the results of the SLNB and the histopathology of the resection specimens of CND. 


Results: post-neoadjuvant patients, the identification rate and false negative rate of each single procedure for SLNB was 84.3% and 5.9% when used Indigo Carmine blue, 94.1% and 0 when used ICG fluorescence, 92.2% and 3.9% when used RI, respectively. In contrast, the total calculation of triple tracer showed that identification rate reached to 96.1% and false negative rate was 0, respectively. 


Conclusions: Our results suggested that the multitracer technique combining blue dye, ICG, and radioisotope is effective method for detection of SLNs in post-neoadjuvant cN+ BC pts. The identification rate and false negative rate of SLNB might be improved by this multiple tracer mapping technique, particularly for patients with ypN(+) after NAC. It is considered that the multi-tracer can complement each other for what was not able to be traced and detected by the single tracer with one mapping material, and that result in totally the improvement of identification rate of SLNB.

Keywords: breast cancer, neo-adjuvant chemotherapy (NAC), sentinel lymph node biopsy (SLNB)

Article Details

How to Cite
TAKAO, Yuko et al. Multi-tracer sentinel node biopsy for patients with breast cancer after neoadjuvant chemotherapy. Medical Research Archives, [S.l.], v. 11, n. 12, dec. 2023. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/4688>. Date accessed: 15 may 2024. doi: https://doi.org/10.18103/mra.v11i12.4688.
Section
Research Articles

References

1. Lyman GH, Giuliano AE, Somerfield MR et al. American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. Journal of clinical oncology 2005;23(30):7703-20. doi: 10.1200/JCO.2005.08.001

2. Buchholz TA, Lehman CD, Harris JR,et al. Statement of the science concerning locoregional treatments after preoperative chemotherapy for breast cancer: National Cancer Institute conference. Journal of clinical oncology 2008;26(5):791-797. doi: 10.1200/JCO.2007.15.0326

3. 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. Journal of clinical oncology 2017;35(5):561-564. doi: 10.1200/JCO.2016.71.0947

4. Xing Y, Foy M, Cox,DD,KuererHM,Hunt KK, Cormier JN. Meta-analysis of sentinel lymph node biopsy after preoperative chemotherapy in patients with breast cancer. The British journal of surgery 2006;93(5):539-546.
doi: 10.1002/bjs.5209

5. van Deurzen CH, Vriens BE, Tjan-Heijnen VC, et al. Accuracy of sentinel node biopsy after neoadjuvant chemotherapy in breast cancer patients: a systematic review. European journal of cancer (Oxford, England: 1990). 2009;45(18):3124-3130. doi: 10.1016/j.ejca.2009.08.001

6. Nason KS, Anderson BO, Byrd DR, et al. Increased false negative sentinel node biopsy rates after preoperative chemotherapy for invasive breast carcinoma. Cancer. 2000;89(11):2187-2194. https://pubmed.ncbi.nlm.nih.gov/11147588/

7. Brady EW. Sentinel lymph node mapping following neoadjuvant chemotherapy for breast cancer. The breast journal. 2002;8(2): 97-100. doi: 10.1046/j.1524-4741.2002.08205.x

8. El Hage Chehade H, Headon H, El Tokhy,Heeney J,Kasem A, Mokbel K.Is sentinel lymph node biopsy a viable alternative to complete axillary dissection following neoadjuvant chemotherapy in women with node-positive breast cancer at diagnosis? An updated meta-analysis involving 3,398 patients. American journal of surgery. 2016;212(5):969-981. doi: 10.1016/j.amjsurg.2016.07.018

9. Tee SR, Devane LA, Evoy D, et al. Meta-analysis of sentinel lymph node biopsy after neoadjuvant chemotherapy in patients with initial biopsy-proven node-positive breast cancer. The British journal of surgery. 2018;105(12):1541-1552. doi: 10.1002/bjs.10986

10. Montagna G, Mamtani A ,Knezevic A,Brogi E, Barrio AV, Monica Morrow.Selecting Node-Positive Patients for Axillary Downstaging with Neoadjuvant Chemotherapy. Annals of surgical oncology. 2020;27(11):4515-4522. doi: 10.1245/s10434-020-08650-z

11. Wong SM, Weiss A, Mittendorf EA, King TA, Golshan M. Surgical Management of the Axilla in Clinically Node-Positive Patients Receiving Neoadjuvant Chemotherapy: A National Cancer Database Analysis. Annals of surgical oncology. 2019;26(11):3517-3525. doi: 10.1245/s10434-019-07583-6

12. Caudle AS, Bedrosian I, Milton DR,et al. Use of Sentinel Lymph Node Dissection After Neoadjuvant Chemotherapy in Patients with Node-Positive Breast Cancer at Diagnosis: Practice Patterns of American Society of Breast Surgeons Members. Annals of surgical oncology. 2017;24(10):2925-2934.
doi: 10.1245/s10434-017-5958-4

13. Nguyen TT, Hoskin TL, Day CN, et al. Decreasing Use of Axillary Dissection in Node-Positive Breast Cancer Patients Treated with Neoadjuvant Chemotherapy. Annals of surgical oncology.2018;25(9):2596-2602.
doi: 10.1245/s10434-018-6637-9

14. Micco RD, Zuber V, Fiacco E, et al. Corrigendum to "Sentinel node biopsy after primary systemic therapy in node positive breast cancer patients: Time trend, imaging staging power and nodal downstaging according to molecular subtype". European journal of surgical oncology. 2019;45(9):1754. doi: 10.1016/j.ejso.2019.07.007

15. Sharkey FE, Addington SL, Fowler LJ, Page CP, Cruz AB. Effects of preoperative chemotherapy on the morphology of resectable breast carcinoma. Modern pathology. 1996;9(9):893-900. https://pubmed.ncbi.nlm.nih.gov/8878021/

16. Fisher ER, Wang J, Bryant J, Fisher B, Eletherios Mamounas, Norman Wolmark. Pathobiology of preoperative chemotherapy: findings from the National Surgical Adjuvant Breast and Bowel (NSABP) protocol B-18. Cancer. 2002;95(4):681-95. doi: 10.1002/cncr.10741

17. Qu LT, Peters S, Cobb AN, Godellas CD, Perez CB, Vaince FT. Considerations for sentinel lymph node biopsy in breast cancer patients with biopsy proven axillary disease prior to neoadjuvant treatment. American journal of surgery. 2018;215(3):530-533. doi:10.1016/j.amjsurg.2017.11.015

18. Boughey JC, Suman VJ, Mittendorf EA ,et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA.2013;310(14):1455-61. doi: 10.1001/jama.2013.278932

19. Boughey JC, Suman VJ, Mittendorf EA, et al. Factors affecting sentinel lymph node identification rate after neoadjuvant chemotherapy for breast cancer patients enrolled in ACOSOG Z1071 (Alliance). Annals of surgery. 2015;261(3):547-52. doi: 10.1097/SLA.0000000000000551

20. Kuehn T, Bauerfeind I, Fehm T, et al. Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study. The Lancet Oncology. 2013;14(7):609-18. doi: 10.1016/S1470-2045(13)70166-9

21. Fu JF, Chen HL, Yang J, Yi CH ,Zheng S. Feasibility and accuracy of sentinel lymph node biopsy in clinically node-positive breast cancer after neoadjuvant chemotherapy: a meta-analysis. PloS one. 2014;9(9): e105316. doi: 10.1371/journal.pone.0105316

22. Boileau JF, Poirier B, Basik M, et al. Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study. Journal of clinical oncology. 2015;33(3):258-64.
doi: 10.1200/JCO.2014.55.7827

23. Toh U, Iwakuma N, Mishima M, Okabe M, Nakagawa S, Akagi Y. Navigation surgery for intraoperative sentinel lymph node detection using Indocyanine green (ICG) fluorescence real-time imaging in breast cancer. Breast cancer research and treatment. 2015;153(2):337-44. doi: 10.1007/s10549-015-3542-9
24. Sugie T, Ikeda T, Kawaguchi A, Shimizu A, Toi M. Sentinel lymph node bopsy using indocyanine green fluorescence in early-stage breast cancer: a meta-analysis. International journal of clinical oncology. 2017;22(1):11-17. doi: 10.1007/s10147-016-1064-z

25. Goonawardena J, Yong C, Law M. Use of indocyanine green fluorescence compared to radioisotope for sentinel lymph node biopsy in early-stage breast cancer: systematic review and meta-analysis. American journal of surgery. 2020;220(3):665-76. doi: 10.1016/j.amjsurg.2020.02.001

26. Brown AS, Hunt KK, Shen J, et al. Histologic changes associated with false-negative sentinel lymph nodes after preoperative chemotherapy in patients with confirmed lymph node-positive breast cancer before treatment. Cancer. 2010;116(12):2878-83. doi: 10.1002/cncr.25066

27. Charfare H, Limongelli S, Purushotham AD. Neoadjuvant chemotherapy in breast cancer. The British journal of surgery. 2005;92(1):14-23. doi: 10.1002/bjs.4840

28. Gimbergues P, Abrial C, Durando X, et al. Sentinel lymph node biopsy after neoadjuvant chemotherapy is accurate in breast cancer patients with a clinically negative axillary nodal status at presentation. Annals of surgical oncology. 2008;15(5):1316-21. doi: 10.1245/s10434-007-9759-z

29. Pilewskie M, Morrow M, Axillary Nodal Management Following Neoadjuvant Chemotherapy: A Review. JAMA oncology. 2017;3(4):549-55. doi: 10.1001/jamaoncol.2016.4163

30. Barrio AV, Mamtani A, Edelweiss M,et al. How Often Is Treatment Effect Identified in Axillary Nodes with a Pathologic Complete Response After Neoadjuvant Chemotherapy? Annals of surgical oncology. 2016;23(11):3475-80. doi: 10.1245/s10434-016-5463-1

31. Tsuyuki S, Yamaguchi A, Kawata Y, Kawaguchi K. Assessing the effects of neoadjuvant chemotherapy on lymphatic pathways to sentinel lymphnodes in cases of breast cancer: Usefulness of the indocyanine green-fluorescence method. Breast (Edinburgh, Scotland). 2015;24(3):298-301. doi: 10.1016/j.breast.2015.02.034

32. Tsopelas C. Particle size analysis of (99m)Tc-labeled and unlabeled antimony trisulfide and rhenium sulfide colloids intended for lymphoscintigraphic application. Journal of nuclear medicine. 2001;42(3):460-6. https://pubmed.ncbi.nlm.nih.gov/11337524/

33. Alazraki NP, Eshima D, Eshima LA,et al. Lymphoscintigraphy, the sentinel node concept, and the intraoperative gamma probe in melanoma, breast cancer, and other potential cancers. Seminars in nuclear medicine. 1997;27(1):55-67. doi: 10.1016/s0001-2998(97)80036-0

34. Tsopelas C,Sutton R. Why certain dyes are useful for localizing the sentinel lymph node. Journal of nuclear medicine. 2002;43(10):1377-82. https://pubmed.ncbi.nlm.nih.gov/12368377/

35. Mathelin C, Lodi M. Narrative review of sentinel lymph node biopsy in breast cancer: a technique in constant evolution with still numerous unresolved questions. Chinese clinical oncology. 2020.
doi: 10.21037/cco-20-207

36. Weiler M, Kassis T, Dixon JB. Sensitivity analysis of near-infrared functional lymphatic imaging. Journal of biomedical optics. 2012;17(6):066019.
doi: 10.1117/1.JBO.17.6.066019

37.Bar-David S, Larush L, Goder N, et al. Size and lipid modification determine liposomal Indocyanine green performance for tumor imaging in a model of rectal cancer. Scientific reports. 2019;9(1):8566.
doi: 10.1038/s41598-019-45038-w

38. Rodier JF, Velten M, Wilt M, et al. Prospective multicentric randomized study comparing periareolar and peritumoral injection of radiotracer and blue dye for the detection of sentinel lymph node in breast sparing procedures: FRANSENODE trial. Journal of clinical oncology. 2007;25(24):3664-9.
doi: 10.1200/JCO.2006.08.4228

39. Canavese G, Gipponi M, Catturich A, et al. Technical issues and pathologic implications of sentinel lymph node biopsy in early-stage breast cancer patients. Journal of surgical oncology. 2001;77(2):81-7.
doi: 10.1002/jso.1074

40. Takao Y, Toh U, Sakurai S, et al. Triple-Tracer Technique of Sentinel Lymph Node Biopsy Using Blue Dye plus Radioisotope Combined with Real-Time Indocyanine Green (ICG)Fluorescence Imaging Procedures for Patients with Breast Cancer Treated with Neoadjuvant Chemotherapy. Article in Japanese.Gan to kagaku ryoho Cancer & chemotherapy. 2020;47(8):1225-7. https://pubmed.ncbi.nlm.nih.gov/32829360/

41. Caudle AS,Y ang WT, Krishnamurthy S, et al. Improved Axillary Evaluation Following Neoadjuvant Therapy for Patients With Node-Positive Breast Cancer Using Selective Evaluation of Clipped Nodes: Implementation of Targeted Axillary Dissection. Journal of clinical oncology. 2016;34(10):1072-8.
doi: 10.1200/JCO.2015.64.0094

42. Straver ME, Loo CE, Alderliesten T, Rutgers EJ, Vrancken Peeters MT. Marking the axilla with radioactive iodine seeds (MARI procedure) may reduce the need for axillary dissection after neoadjuvant chemotherapy for breast cancer. The British journal of surgery. 2010;97(8):1226-1231. doi: 10.1002/bjs.7073

43. Koolen BB ,Donker M, Straveret ME, et al. Combined PET-CT and axillary lymph node marking with radioactive iodine seeds (MARI procedure) for tailored axillary treatment in node-positive breast cancer after neoadjuvant therapy. The British journal of surgery. 2017;104(9):1188-96. doi: 10.1002/bjs.10555

44. van der Noordaa MEM, van Duijnhoven FH, Straver ME, et al. Major Reduction in Axillary Lymph Node Dissections After Neoadjuvant Systemic Therapy for Node-Positive Breast Cancer by combining PET/CT and the MARI Procedure. Annals of surgical oncology. 2018;25(6):1512-20.
doi: 10.1245/s10434-018-6404-y