Skip to main content

Advertisement

SpringerLink
Log in

Impact of the extent of axillary surgery in patients with N2–3 disease in the de-escalation era: a propensity score-matched study

  • Research Article
  • Published:
Clinical and Translational Oncology Aims and scope Submit manuscript

Abstract

Background

Reduction of surgeries in axillary has been proved feasible in breast cancer with negative and limited involved axillary lymph nodes. However, for women with a heavy axillary burden, the extent of dissection is still arguable.

Patients and methods

From a total of 7042 patients with breast cancer who underwent surgical treatments between 2008 and 2014, 692 (9.85%) patients with the axillary staging of N2–3M0 were classified into Level I–II dissection group and Level I–III dissection group. 203 pairs of patients were matched by the propensity score.

Results

The positive rate of level-III lymph nodes is 62.4% in patients who underwent Level I–III dissection. There are 67 (22.1%) patients who experienced rise in staging from N2 to N3 due to level-III dissection. With a median follow-up of 62.4 months, no significant difference was observed in RFS (P = 0.897), MFS (P = 0.610) and OS (P = 0.755) between level I–II group and level I–III group. The same results were observed in the independent analysis of neoadjuvant and non-neoadjuvant subgroups. The binary regression model showed the positivity of level-III is only associated with involved lymph nodes in level-II.

Conclusion

Additional level-III dissection has a limited impact on survival but still valuable in an accurate stage. The reduction of surgeries in axillary should be treated with discretion in breast cancer patients with a heavy axillary burden.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Giuliano AE, Jones RC, Brennan M, Statman R. Sentinel lymphadenectomy in breast cancer. J Clin Oncol: Off J Am Soc Clin Oncol. 1997;15(6):2345–50. https://doi.org/10.1200/JCO.1997.15.6.2345.

    Article  CAS  Google Scholar 

  2. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220(3):391–8. https://doi.org/10.1097/00000658-199409000-00015(discussion 8-401).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Giuliano AE, Ballman KV, McCall L, Beitsch PD, Brennan MB, Kelemen PR, et al. Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: the ACOSOG Z0011 (Alliance) randomized clinical trial. JAMA. 2017;318(10):918–26. https://doi.org/10.1001/jama.2017.11470.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Galimberti V, Cole BF, Viale G, Veronesi P, Vicini E, Intra M, et al. Axillary dissection versus no axillary dissection in patients with breast cancer and sentinel-node micrometastases (IBCSG 23-01): 10-year follow-up of a randomised, controlled phase 3 trial. Lancet Oncol. 2018;19(10):1385–93. https://doi.org/10.1016/S1470-2045(18)30380-2.

    Article  PubMed  Google Scholar 

  5. Gradishar WJ, Anderson BO, Balassanian R, Blair SL, Burstein HJ, Cyr A, et al. Breast cancer, version 1.2016. JNCCN. 2015;13(12):1475–85.

    CAS  PubMed  Google Scholar 

  6. Nouso K, Miyahara K, Uchida D, Kuwaki K, Izumi N, Omata M, et al. Effect of hepatic arterial infusion chemotherapy of 5-fluorouracil and cisplatin for advanced hepatocellular carcinoma in the Nationwide Survey of Primary Liver Cancer in Japan. Br J Cancer. 2013;109(7):1904–7. https://doi.org/10.1038/bjc.2013.542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Telli ML, Gradishar WJ, Ward JH. NCCN guidelines updates: breast cancer. JNCCN. 2019;17(5.5):552–5. https://doi.org/10.6004/jnccn.2019.5006.

    Article  PubMed  Google Scholar 

  8. Cardoso F, Senkus E, Costa A, Papadopoulos E, Aapro M, Andre F, et al. 4th ESO-ESMO international consensus guidelines for advanced breast cancer (ABC 4)dagger. Ann Oncol: Off J Eur Soc Med cal Oncol/ESMO. 2018;29(8):1634–57. https://doi.org/10.1093/annonc/mdy192.

    Article  CAS  Google Scholar 

  9. Orr RK. The impact of prophylactic axillary node dissection on breast cancer survival–a Bayesian meta-analysis. Ann Surg Oncol. 1999;6(1):109–16.

    Article  CAS  Google Scholar 

  10. Wright FC, Walker J, Law CH, McCready DR. Outcomes after localized axillary node recurrence in breast cancer. Ann Surg Oncol. 2003;10(9):1054–8.

    Article  CAS  Google Scholar 

  11. Konkin DE, Tyldesley S, Kennecke H, Speers CH, Olivotto IA, Davis N. Management and outcomes of isolated axillary node recurrence in breast cancer. Archives of surgery. 2006;141(9):867–72. https://doi.org/10.1001/archsurg.141.9.867(discussion 72-4).

    Article  PubMed  Google Scholar 

  12. Dillon MF, Advani V, Masterson C, O’Loughlin C, Quinn CM, O’Higgins N, et al. The value of level III clearance in patients with axillary and sentinel node positive breast cancer. Ann Surg. 2009;249(5):834–9. https://doi.org/10.1097/SLA.0b013e3181a40821.

    Article  PubMed  Google Scholar 

  13. Yildirim E, Berberoglu U. Lymph node ratio is more valuable than level III involvement for prediction of outcome in node-positive breast carcinoma patients. World J Surg. 2007;31(2):276–89. https://doi.org/10.1007/s00268-006-0487-5.

    Article  PubMed  Google Scholar 

  14. Kodama H, Nio Y, Iguchi C, Kan N. Ten-year follow-up results of a randomised controlled study comparing level-I vs level-III axillary lymph node dissection for primary breast cancer. Br J Cancer. 2006;95(7):811–6. https://doi.org/10.1038/sj.bjc.6603364.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Park TS, Thomas SM, Rosenberger LH, Fayanju OM, Plichta JK, Blitzblau RC, et al. The association of extent of axillary surgery and survival in women with N2-3 invasive breast cancer. Ann Surg Oncol. 2018;25(10):3019–29. https://doi.org/10.1245/s10434-018-6587-2.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Lilleborge M, Falk RS, Russnes H, Sauer T, Ursin G, Hofvind S. Risk of breast cancer by prior screening results among women participating in Breast Screen Norway. Cancer. 2019. https://doi.org/10.1002/cncr.32330.

    Article  PubMed  Google Scholar 

  17. Lin CH, Yap YS, Lee KH, Im SA, Naito Y, Yeo W, et al. Contrasting epidemiology and clinicopathology of female breast cancer in asians versus the US population. J Natl Cancer Inst. 2019. https://doi.org/10.1093/jnci/djz090.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Mori M, Fujimori M, van Vliet LM, Yamaguchi T, Shimizu C, Kinoshita T, et al. Explicit prognostic disclosure to Asian women with breast cancer: a randomized, scripted video-vignette study (J-SUPPORT1601). Cancer. 2019. https://doi.org/10.1002/cncr.32327.

    Article  PubMed  Google Scholar 

  19. Kong Y, Yang L, Tang H, Lv N, Xie X, Li J, et al. A nation-wide multicenter retrospective study of the epidemiological, pathological and clinical characteristics of breast cancer in situ in Chinese women in 1999–2008. PLoS ONE. 2013;8(11):e81055. https://doi.org/10.1371/journal.pone.0081055.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Early Breast Cancer Trialists’ Collaborative G. Long-term outcomes for neoadjuvant versus adjuvant chemotherapy in early breast cancer: meta-analysis of individual patient data from ten randomised trials. Lancet Oncol. 2018;19(1):27–39. https://doi.org/10.1016/s1470-2045(17)30777-5.

    Article  CAS  Google Scholar 

  21. Pelizzari G, Gerratana L, Basile D, Fanotto V, Bartoletti M, Liguori A, et al. Post-neoadjuvant strategies in breast cancer: from risk assessment to treatment escalation. Cancer Treat Rev. 2019;72:7–14. https://doi.org/10.1016/j.ctrv.2018.10.014.

    Article  PubMed  Google Scholar 

  22. Bonneau C, Hequet D, Estevez JP, Pouget N, Rouzier R. Impact of axillary dissection in women with invasive breast cancer who do not fit the Z0011 ACOSOG trial because of three or more metastatic sentinel lymph nodes. Eur J Surg Oncol: J Eur Soc Surg Oncol Br Assoc Surg Oncol. 2015;41(8):998–1004. https://doi.org/10.1016/j.ejso.2015.04.003.

    Article  CAS  Google Scholar 

  23. Steenbruggen TG, Steggink LC, Seynaeve CM, van der Hoeven JJM, Hooning MJ, Jager A, et al. High-dose chemotherapy with hematopoietic stem cell transplant in patients with high-risk breast cancer and 4 or more involved axillary lymph nodes: 20-year follow-up of a phase 3 randomized clinical trial. JAMA Oncol. 2020;6(4):528–34. https://doi.org/10.1001/jamaoncol.2019.6276.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Author notes

  1. Y. Kong and A. Yang have contributed equally to this study.

Authors and Affiliations

  1. State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Department of Breast Oncology, Sun Yat-sen University Cancer Center, 651 Dongfeng Road East, Guangzhou, 510060, Guangdong, People’s Republic of China

    Y. Kong, A. Yang, X. Xie, J. Zhang, H. Xu & W. Wei

  2. Department of Pathology and Laboratory Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    M. Li

  3. State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Department of Minimally Invasive Interventional Radiology, Sun Yat-sen University Cancer Center, 651 Dongfeng Road East, Guangzhou, 510060, Guangdong, People’s Republic of China

    N. Lyu

Authors
  1. Y. Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. X. Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. H. Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. N. Lyu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. W. Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to N. Lyu or W. Wei.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

This retrospective study was approved by the Ethical Review Committee of Sun Yat-sen University Cancer Center and conducted following the principles of the Declaration of Helsinki. Nine hundred and forty-five consecutive female patients diagnosed with pathologic N2–3 (pN2–3) invasive breast cancer between October 2008 and December 2014 were identified from a total of 7042 patients with breast cancer in the Sun Yat-Sen University Cancer Center Database.

Informed consent

Patients’ informed consent was obtained before conducting the treatment.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

12094_2020_2444_MOESM1_ESM.tif

Figure S1—Kaplan–Meier curves for locoregional recurrence-free survival (RFS), distant metastasis-free survival (MFS) and overall survival (OS) in L-II group and L-III group before match. A, C, and E: neoadjuvant population and, B, D and F: non-adjuvant population. Supplementary material 1 (TIFF 155 kb)

12094_2020_2444_MOESM2_ESM.tif

Figure S2—Kaplan–Meier locoregional RFS curves in the subgroups of level III lymph nodes resected population. Supplementary material 2 (TIFF 1737 kb)

12094_2020_2444_MOESM3_ESM.tif

Figure S3—Kaplan–Meier distant MFS curves in the subgroups of level III lymph nodes resected population. Supplementary material 3 (TIFF 1892 kb)

12094_2020_2444_MOESM4_ESM.tif

Figure S4—Kaplan–Meier OS curves in the subgroups of level III lymph nodes resected population. Supplementary material 4 (TIFF 1788 kb)

Supplementary material 5 (DOCX 27 kb)

Supplementary material 6 (DOCX 20 kb)

Supplementary material 7 (DOCX 19 kb)

Supplementary material 8 (DOCX 23 kb)

Supplementary material 9 (DOCX 20 kb)

Supplementary material 10 (DOCX 19 kb)

Supplementary material 11 (DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kong, Y., Yang, A., Xie, X. et al. Impact of the extent of axillary surgery in patients with N2–3 disease in the de-escalation era: a propensity score-matched study. Clin Transl Oncol 23, 526–535 (2021). https://doi.org/10.1007/s12094-020-02444-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12094-020-02444-1

Keywords

Search

Navigation