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Management of the axilla in breast cancer: outcome analysis in a series of ductal versus lobular invasive cancers

Abstract

Introduction

Axillary lymph node dissection (ALND) has been considered essential for the staging of breast cancer (BC). As the impact of tumor biology on clinical outcomes is recognized, a surgical de-escalation approach is being implemented. We performed a retrospective study focused on surgical management of the axilla in invasive lobular carcinoma (ILC) versus invasive ductal carcinoma (IDC).

Materials and methods

1151 newly diagnosed BCs, IDCs (79.6%) or ILCs (20.4%), were selected among patients treated at our Breast Cancer Unit from 2012 to 2018. Tumor characteristics and clinical information were collected and predictors of further metastasis after positive sentinel lymph node biopsy (SLNB) analyzed in relation to disease-free survival (DFS) and overall survival (OS).

Results

27.5% of patients with ILC had ≥ 3 metastatic lymph nodes at ALND after positive SLNB versus 11.48% of IDCs (p = 0.04). Risk predictors of further metastasis at ALND were the presence of > 2 positive lymph nodes at SLNB (OR = 4.72, 95% CI 1.15–19.5 p = 0.03), T3–T4 tumors (OR = 4.93, 95% CI 1.10–22.2, p = 0.03) and Non-Luminal BC (OR = 2.74, 95% CI 1.16–6.50, p = 0.02). The lobular histotype was not associated with the risk of further metastasis at ALND (OR = 1.62, 95% CI 0.77–3.41, p = 0.20).

Conclusions

ILC histology is not associated with higher risk of further metastasis at ALND in our analysis. However, surgical management decisions should be taken considering tumor histotype, biology and expected sensitivity to adjuvant therapies.

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References

  1. 1.

    Lowery AJ, Kell MR, Glynn RW et al (2012) Locoregional recurrence after breast cancer surgery: a systematic review by receptor phenotype. Breast Cancer Res Treat 133(3):831–841

  2. 2.

    Lucci A, Mc Call LM, Beitsch PD et al (2007) American College of Surgeons Oncology Group: surgical complication associated with sentinel lymph node dissection (SLND) plus axillary lymph node dissection compared with SLND alone in the American College of Surgeons Oncology Group Trial Z0011. J Clin Oncol 25(24):3657–3663

  3. 3.

    Biglia N, Maggiorotto F, Liberale V et al (2013) Clinical-pathologic features, long term-outcome and surgical treatment in a large series of patients with invasive lobular carcinoma (ILC) and invasive ductal carcinoma (IDC). Eur J Surg Oncol 39(5):455–460. https://doi.org/10.1016/j.ejso.2013.02.007

  4. 4.

    Giuliano AE, Ballman KV, McCall L et al (2017) 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 318:918–925

  5. 5.

    Fisher B, Anderson S, Bryant J et al (2002) Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med 347:1233–1241

  6. 6.

    Mansel RE, Fallowfield L, Kissin M et al (2006) Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial. J NatlCancerInst 98:599–609

  7. 7.

    Veronesi U, Viale G, Paganelli G et al (2010) Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study. Ann Surg 251:595–600

  8. 8.

    Krag DN, Anderson SJ, Julian TB et al (2010) Sentinel lymph-node resection compared with conventional axillary lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomized phase 3 trial. Lancet Oncol 11:927–933

  9. 9.

    Giuliano AE, Hunt KK, Ballman KV et al (2011) Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 305:569–575

  10. 10.

    de Boer M, Van Deurzen CHM, Van Dijck JAAM et al (2009) Micrometastases or isolated tumor cells and the outcome of breast cancer. N Eng J Med 361:653–663. https://doi.org/10.1056/NEJMoa0904832

  11. 11.

    Weaver DL, Ashikaga T, Krag DN et al. Effect of occult metastases on survival in node-negative breast cancer. N Engl J Med 2011; 364:412–421.

  12. 12.

    Bello DM, Russell C, McCullough D et al (2018) Lymph node status in breast cancer does not predict tumor biology. Ann Surg Oncol 25(10):2884–2889. https://doi.org/10.1245/s10434-018-6598-z.520

  13. 13.

    Petkov VI, Miller DP, Howlader N et al (2016) Breast-cancer-specific mortality in patients treated based on the 21-gene assay: a SEER population-based study [published correction appears in NPJ breast cancer 2018 Jul 6;4:17]. NPJ Breast Cancer 2:16017. https://doi.org/10.1038/npjbcancer.2016.17

  14. 14.

    Bevilacqua JL, Kattan MW, Fey JV et al (2007) Doctor, what are my chances of having a positive sentinel node? A validated nomogram for risk estimation. J Clin Oncol 25:3670–3679

  15. 15.

    Chen JY, Chen JJ, Yang BL, et al. Predicting sentinel lymph node metastasis in a Chinese breast cancer population: assessment of an existing nomogram and a new predictive nomogram. Breast Canc Res Treat 2012;135:839e48

  16. 16.

    Yeniay L, Carti E, Karaca C et al (2012) A new and simple predictive formula for nonsentinel lymph node metastasis in breast cancer patients with positive sentinel lymph nodes, and validation of 3 different nomograms in Turkish breast cancer patients. Breast Care 7:397–402

  17. 17.

    Coombs N, Chen W, Taylor R, Boyages J (2007) A decision tool for predicting sentinel node accuracy from breast tumor size and grade. Breast J 13:593–598

  18. 18.

    Elmadahma A, Lord SJ, Hudson HM et al (2018) Performance of four published risk models to predict sentinel lymph-node involvement in Australian women with early breast cancer. Breast 41:82–88. https://doi.org/10.1016/j.breast.2018.05.011)

  19. 19.

    Fernandez B, Paish EC, Green AR et al. Lymph-node metastases in invasive lobular carcinoma are different from those in ductal carcinoma of the breast. J Clin Pathol 2011;64:995–1000

  20. 20.

    Adachi Y, Sawaki M, Hattori M et al (2018) Comparison of sentinel lymph node biopsy between invasive lobular carcinoma and invasive ductal carcinoma. Breast Cancer 25:560–565. https://doi.org/10.1007/s12282-018-0852-x

  21. 21.

    Roberts A, Nofech-Mozes S, Youngson B et al (2015) The importance of applying ACOSOG Z0011 criteria in the axillary management of invasive lobular carcinoma: a multi-institutional cohort study. Ann SurgOncol 22:3397–3401. https://doi.org/10.1245/s10434-015-4756-0

  22. 22.

    Gebhardt BJ, Thomas J, Horne ZD et al. Is completion axillary lymph node dissection necessary in patients who are underrepresented in the ACOSOG Z0011 trial? Adv Radiat Oncol 2018:3(3): 258–264.doi: 10.1016/j.adro.2018.03.004.

  23. 23.

    Caudle AS, Kuerer HM, Le-Petross HT et al (2014) Predicting the extent of nodal disease in early-stage breast cancer. Ann Surg Oncol 21:3440–3447. https://doi.org/10.1245/s10434-014-3813-4

  24. 24.

    Donker M, van Tienhoven G, Straver ME et al (2014) Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981–22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol 15:1303–1310

  25. 25.

    Adachi Y, Ishiguro J, Kotani H et al (2016) Comparison of clinical outcomes between luminal invasive ductal carcinoma and luminal invasive lobular carcinoma. BMC Cancer 16:248

  26. 26.

    Van Wyhe RD, Claudle AS, Shaitelman SF et al (2018) A component of lobular carcinoma in clinically lymph node–negative patients predicts for an increased likelihood of upstaging to pathologic stage III breast cancer. Advances in Radiation Oncology 3:252–257

  27. 27.

    Arpino G, Bardou VJ, Clark GM et al (2004) Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cancer Res 6:R149–R156

  28. 28.

    Li CI, Uribe DJ, Daling JR (2005) Clinical characteristics of different histologic types of breast cancer. Br J Cancer 93:1046–1052

  29. 29.

    Weinberg ES, Dickson D, White L et al (2004) Cytokeratin staining for intraoperative evaluation of sentinel lymph nodes in patients with invasive lobular carcinoma. Am J Surg 188:419–422

  30. 30.

    Howard-McNatt M, Geisinger KR, Stewart JHt, Shen P, Levine EA. Is intraoperative imprint cytology evaluation still feasible for the evaluation of sentinel lymph nodes for lobular carcinoma of the breast? Ann Surg Oncol. 2012; 19(3):929–934. https://doi.org/10.1245/s10434-011-2038-z PMID: 21879268

  31. 31.

    Creager AJ, Geisinger KR, Perrier ND, Shen P, Shaw JA, Young PR et al (2004) Intraoperative imprint cytologic evaluation of sentinel lymph nodes for lobular carcinoma of the breast. Ann Surg 239(1):61–66. https://doi.org/10.1097/01.sla.0000103072.34708.e3 PMID: 14685101

  32. 32.

    Tiernan JP, Verghese ET, Nair A et al (2014) Systematic review and meta-analysis of cytokeratin 19-based one-step nucleic acid amplification versus histopathology for sentinel lymph node assessment in breast cancer. Br J Surg 101:298–306 (PMID: 24536007)

  33. 33.

    Wasif N, Maggard MA, Ko CY et al. Invasive lobular vs. ductal breast cancer: a stage-matched comparison of outcomes. Ann Surg Oncol. 2010; 17: 1862–1869

  34. 34.

    Hsiao YH, Tsai HD, Chou MC et al (2011) The myoepithelial cell layer may serve as a potential trigger factor for different outcomes of stage-matched invasive lobular and ductal breast cancers. Int J Biol Sci 7:147–153

  35. 35.

    Goldhirsch A, Winer EP, Coates AS et al (2013) Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the primary therapy of early breast cancer. Ann Oncol 24:2206–2223. https://doi.org/10.1093/annonc/mdt303

  36. 36.

    Truin W, Voogd AC, Vreugdenhil G et al (2012) Effect of adjuvant chemotherapy in postmenopausal patients with invasive ductal versus lobular breast cancer. Ann Oncol 23:2859–2865

  37. 37.

    Davies C, Godwin J, Gray R et al (2011) Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: patient-level metaanalysis of randomised trials. Lancet 378:771–784

  38. 38.

    MetzgerFilho O, Giobbie-Hurder A, Mallon E et al (2015) Relative effectiveness of letrozole compared with tamoxifen for patients with lobular carcinoma in the BIG 1–98 trial. J Clin Oncol 33:2772–2779

  39. 39.

    Rakha EA, Ellis IO (2010) Lobular breast carcinoma and its variants. Semin Diagn Pathol 27:49–61

  40. 40.

    Braunstein LZ, Brock JE, Chen YH et al (2015) Invasive lobular carcinoma of the breast: local recurrence after breast-conserving therapy by subtype approximation and surgical margin. Breast Cancer Res Treat 149:555–564

  41. 41.

    Sagara Y, Barry WT, Mallory MA et al (2015) Surgical options and locoregional recurrence in patients diagnosed with invasive lobular carcinoma of the breast. Ann Surg Oncol 22:4280–4286

  42. 42.

    Stecklein SR, Shen X, Mitchell MP (2016) Post-mastectomy radiation therapy for invasive lobular carcinoma: a comparative utilization and outcomes study. Clin Breast Cancer 16:319–326

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Correspondence to S. P. Corona.

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Conflict of interest

The authors Silvia Paola Corona, Marina Bortul, Serena Scomersi, Chiara Bigal, Fabrizio Zanconati, Stephen Fox, Fabiola Giudici, and Daniele Generali declare that they have no conflict of interest.

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Corona, S.P., Bortul, M., Scomersi, S. et al. Management of the axilla in breast cancer: outcome analysis in a series of ductal versus lobular invasive cancers. Breast Cancer Res Treat (2020). https://doi.org/10.1007/s10549-020-05565-x

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Keywords

  • Invasive lobular carcinoma
  • Invasive ductal carcinoma
  • Axilla
  • Surgical management
  • ALND
  • Breast cancer