Top

Published in:

Open Access 01-12-2024 | Metastasis | Research

Correlation between sentinel lymph node biopsy and non-sentinel lymph node metastasis in patients with cN0 breast carcinoma: comparison of invasive ductal carcinoma and invasive lobular carcinoma

Authors: Calogero Cipolla, Simona Lupo, Nello Grassi, Giuseppe Tutino, Martina Greco, D’Agati Eleonora, Vittorio Gebbia, Maria Rosaria Valerio

Published in: World Journal of Surgical Oncology | Issue 1/2024

Abstract

Background

Some studies have suggested that axillary lymph node dissection (ALND) can be avoided in women with cN0 breast cancer with 1–2 positive sentinel nodes (SLNs). However, these studies included only a few patients with invasive lobular carcinoma (ILC), so the validity of omitting ALDN in these patients remains controversial. This study compared the frequency of non-sentinel lymph nodes (non-SLNs) metastases in ILC and invasive ductal carcinoma (IDC). Materials Methods: Data relating to a total of 2583 patients with infiltrating breast carcinoma operated at our institution between 2012 and 2023 were retrospectively analyzed: 2242 (86.8%) with IDC and 341 (13.2%) with ILC. We compared the incidence of metastasis to SLNs and non-SLNs between the ILC and IDC cohorts and examined factors that influenced non-SLNs metastasis. Results: SLN biopsies were performed in 315 patients with ILC and 2018 patients with IDC. Metastases to the SLNs were found in 78/315 (24.8%) patients with ILC and in 460 (22.8%) patients with IDC (p = 0.31). The incidence of metastases to non-SLNs was significantly higher (p = 0.02) in ILC (52/78–66.7%) compared to IDC (207/460 − 45%). Multivariate analysis showed that ILC was the most influential predictive factor in predicting the presence of metastasis to non-SLNs. Conclusions: ILC cases have more non-SLNs metastases than IDC cases in SLN-positive patients. The ILC is essential for predicting non-SLN positivity in macro-metastases in the SLN. The option of omitting ALND in patients with ILC with 1–2 positive SLNs still requires further investigation.

Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Costantino JP, Ashikaga T, Weaver DL, Mamounas EP, Jalovec LM, Frazier TG, Noyes RD, Robidoux A, Scarth M, Wolmark H. 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 randomised phase 3 trial. Lancet Oncol. 2010;11:927–33. https://doi.org/10.1016/S1470-2045(10)70207-2CrossRefPubMedPubMedCentral

Veronesi U, Paganelli G, Viale G, Luini A, Zurrida S, Galimberti V, Intra M, Veronesi P, Robertson C, Maisonneuve P, Renne G, De Cicco C, De Lucia F. Gennari, R. A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med. 2003;349:546–53. https://doi.org/10.1056/NEJMoa012782CrossRefPubMed

Boler DE, Uras C, Ince U, Cabioglu N. Factors predicting the non-sentinel lymph node involvement in breast cancer patients with sentinel lymph node metastases. Breast. 2012;21:518–23. https://doi.org/10.1016/j.breast.2012.02.012CrossRefPubMed

Giuliano AE, Ballman KV, McCall L, Beitsch PD, Brennan MB, Kelemen PR, Ollila DW, Hansen NM, Whitworth PW, Blumencranz PW, Leitch AM, Saha S, Hunt KK, Morrow M. 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.2017.11470CrossRefPubMedPubMedCentral

Thomas M, Kelly ED, Abraham J, Kruse M. Invasive lobular breast cancer: a review of pathogenesis, diagnosis, management, and future directions of early-stage disease. Semin Oncol. 2019;46:121–32. https://doi.org/10.1053/j.seminoncol.2019.03.002CrossRefPubMed

Hoda SA, Brogi E, Koerner FC, Rosen PP. Rosen’s breast pathology. 4th ed. Philadelphia: Lippincott Williams and Wilkins; 2014. pp. 855–92.

Cristofanilli M, Gonzalez-Angulo A, Sneige N, Kau SW, Broglio K, Theriault RL, Valero V, Buzdar AU, Kuerer H, Buchholz TA, Hortobagyi GN. Invasive lobular carcinoma classic type: response to primary chemotherapy and survival outcomes. J Clin Oncol. 2005;23:41–8. https://doi.org/10.1200/JCO.2005.03.111CrossRefPubMed

Amadori D, Silvestrini R, De Lena M, Boccardo F, Rocca A, Scarpi E, Schittulli F, Brandi M, Maltoni R, Serra P, Ponzone R, Biglia N, Gianni L, Tienghi A, Valerio MR, Bonginelli P, Amaducci L, Faedi M, Baldini E, Paradiso A. Randomized phase III trial of adjuvant epirubicin followed by cyclophosphamide, methotrexate, and 5-fluorouracil (CMF) versus CMF followed by epirubicin in patients with node-negative or 1–3 node-positive rapidly proliferating breast cancer. Breast Cancer Res Treat. 2011;125(3):775–84. https://doi.org/10.1007/s10549-010-1257-5CrossRefPubMed

Roberts A, Nofech-Mozes S, Youngson B, McCready DR, Al-Assi M, Ramkumar S, Cil T. The importance of applying ACOSOG Z0011 criteria in the axillary management of invasive lobular carcinoma: a multi-institutional cohort study. Ann Surg Oncol. 2015;22(10):3397–401. https://doi.org/10.1245/s10434-015-4756-0CrossRefPubMed

10.

Adachi Y, Sawaki M, Hattori M, Yoshimura A, Gondo N, Kotani H, Iwase M, Kataoka A, Onishi S, Sugino K, Terada M, Horisawa N, Mori M, Oze I, Iwata H. Comparison of sentinel lymph node biopsy between invasive lobular carcinoma and invasive ductal carcinoma. Breast Cancer. 2018;25(5):560–5. https://doi.org/10.1007/s12282-018-0852-xCrossRefPubMed

11.

Gao W, Zeng Y, Fei X, Chen X, Shen K. Axillary lymph node and non-sentinel lymph node metastasis among the ACOSOG Z0011 eligible breast cancer patients with invasive ductal, invasive lobular, or other histological special types: a multi-institutional retrospective analysis. Breast Cancer Res Treat. 2020;184:193–202. https://doi.org/10.1007/s10549-020-05842-9CrossRefPubMed

12.

Corona SP, Bortul M, Scomersi S, Scomersi S, Bigal C, Bottin C, Zanconati F, Fox SB, Giudici F, Generali D. Management of the axilla in breast cancer: outcome analysis in a series of ductal versus lobular invasive cancers. Breast Cancer Res Treat. 2020;180:735–45. https://doi.org/10.1007/s10549-020-05565-xCrossRefPubMed

13.

Cipolla C, Fricano S, Vieni S, Amato C, Napoli L, Graceffa G, Latteri S, Latteri MA. Validity of needle core biopsy in the histological characterisation of mammary lesions. Breast. 2006;15(1):76–80. https://doi.org/10.1016/j.breast.2005.01.007CrossRefPubMed

14.

Caruso G, Cipolla C, Costa R, Morabito A, Latteri S, Fricano S, Salerno S, Latteri MA. Lymphoscintigraphy with peritumoral injection versus lymphoscintigraphy with subdermal periareolar injection of technetium-labeled human albumin to identify sentinel lymph nodes in breast cancer patients. Acta Radiol. 2014;55:39–44. https://doi.org/10.1177/0284185113493775CrossRefPubMed

15.

Cipolla C, Vieni S, Fricano S, Cabibi D, Graceffa G, Costa R, Latteri S, Latteri M. The accuracy of sentinel lymph node biopsy in the treatment of multicentric invasive breast cancer using a subareolar injection of tracer. World J Surg. 2008;32:2483–7. https://doi.org/10.1007/s00268-008-9719-1CrossRefPubMed

16.

Cipolla C, Graceffa G, Cabibi D, Gangi G, Latteri M, Valerio MR, Vieni S. Current role of intraoperative frozen section examination of sentinel lymph node in early breast cancer. Anticancer Res. 2020;40:1711–7. https://doi.org/10.21873/anticanres.14124CrossRefPubMed

17.

Pestalozzi BC, Zahrieh D, Mallon E, Gusterson BA, Price KN, Gelber RD, Holmberg SB, Lindtner J, Snyder R, Thürlimann B, Murray E, Viale G, Castiglione-Gertsch M, Coates AS, Goldhirsch A. International breast Cancer Study. Distinct clinical and prognostic features of infiltrating lobular carcinoma of the breast: combined results of 15 international breast Cancer Study Group clinical trials. J Clin Oncol. 2008;26:3006–14. https://doi.org/10.1200/JCO.2007.14.9336CrossRefPubMed

18.

Arpino G, Bardou VJ, Clark GM, Elledge RM. Infiltrating lobular carcinoma of the breast: tumor characteristics and clinical outcome. Breast Cance R Res. 2004;6:149–56. https://doi.org/10.1186/bcr767CrossRef

19.

Cazzaniga ME, Airoldi M, Arcangeli V, Artale S, Atzori F, Ballerio A, et al. Efficacy and safety of everolimus and exemestane in hormone-receptor positive (HR+) human-epidermal-growth-factor negative (HER2–) advanced breast cancer patients: new insights beyond clinical trials. EVA Study Breast. 2017;35:115–21. https://doi.org/10.1016/j.breast.2017.06.043CrossRefPubMed

20.

Lambert LA, Ayers GD, Meric-Bernstam F. Validation of a breast cancer nomogram for predicting non-sentinel lymph node metastases after a positive sentinel node biopsy. Ann Surg Oncol. 2007;14:2422–3. https://doi.org/10.1245/s10434-007-9419-3CrossRefPubMed

21.

Krasniqi E, Pizzuti L, Barchiesi G, Sergi D, Carpano S, Botti C. Impact of BMI on HER2 + metastatic breast cancer patients treated with pertuzumab and/or trastuzumab emtansine. Real-world evidence. J Cell Physiol. 2020;235(11):7900–10. https://doi.org/10.1002/jcp.29445CrossRefPubMed

22.

Fernández B, Paish EC, Green AR, Lee AH, Macmillan RD, Ellis IO, Rakha EA. Lymph-node metastases in invasive lobular carcinoma are different from those in ductal carcinoma of the breast. J Clin Pathol. 2011;64:995–1000. https://doi.org/10.1136/jclinpath-2011-200151CrossRefPubMed

23.

Majid S, Rydén L, Manjer J. Determinants for non-sentinel node metastases in primary invasive breast cancer: a population-based cohort study of 602 consecutive patients with sentinel node metastases. BMC Cancer. 2019;19(1):626. https://doi.org/10.1186/s12885-019-5823-xCrossRefPubMedPubMedCentral

24.

Corona SP, Bortul M, Scomersi S, Bigal C, Bottin C, Zanconati F, Fox SB, Giudici F, Generali D. Management of the axilla in breast cancer: outcome analysis in a series of ductal versus lobular invasive cancers. Breast Cancer Res Treat. 2020;180:735–45. https://doi.org/10.1007/s10549-020-05565-xCrossRefPubMed

25.

Viale G, Maiorano E, Pruneri G, Mastropasqua MG, Valentini S, Galimberti V, Zurrida S, Maisonneuve P, Paganelli G, Mazzarol G. Predicting the risk for additional axillary metastases in patients with breast carcinoma and positive sentinel lymph node biopsy. Ann Surg. 2005;241:319–25. https://doi.org/10.1097/01.sla.0000150255.30665.52CrossRefPubMedPubMedCentral

26.

Christgen M, Derksen P. Lobular breast cancer: molecular basis, mouse and cellular models. Breast Cancer Res. 2015;17:16. https://doi.org/10.1186/s13058-015-0517-zCrossRefPubMedPubMedCentral

27.

Kohrt HE, Olshen RA, Bermas HR, Goodson WH, Wood DJ, Henry S, Rouse RV, Bailey L, Philben VJ, Dirbas FM, Dunn JJ, Johnson DL, Wapnir IL, Carlson RW, Stockdale FE, Hansen NM, Jeffrey SS. & Bay Area SLN Study. New models and online calculator for predicting non-sentinel lymph node status in sentinel lymph node positive breast cancer patients. BMC Cancer. 2008;8:66. https://doi.org/10.1186/1471-2407-8-66CrossRefPubMedPubMedCentral

28.

Abdessalam SF, Zervos EE, Prasad M, Farrar WB, Yee LD, Walker MJ, Carson WB, Burak WE. Jr. Predictors of positive axillary lymph nodes after sentinel lymph node biopsy in breast cancer. Am J Surg. 2001;182:316–20. https://doi.org/10.1016/s0002-9610(01)00719-xCrossRefPubMed

29.

Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJ, Mansel RE, Cataliotti L, Westenberg AH, Klinkenbijl JH, Orzalesi L, Bouma WH, van der Mijle HC, Nieuwenhuijzen GA, Veltkamp SC, Slaets L, Duez NJ, de Graaf PW, van Dalen T, Marinelli A, Rijna H, Snoj M, Bundred NJ, Merkus JW, Belkacemi Y, Petignat P, Schinagl DA, Coens C, Messina CG, Bogaerts J, Rutgers EJ. 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 noninferiority trial. Lancet Oncol. 2014;15:1303–10. https://doi.org/10.1016/S1470-2045(14)70460-7CrossRefPubMedPubMedCentral

30.

Zhang J, Ling Y, Wang T, Yan C, Huang M, Fan Z, Ling R. Chinese Society of Breast Cancer. Analysis of sentinel lymph node biopsy and non-sentinel lymph node metastasis in invasive ductal and invasive lobular breast cancer: a nationwide cross-sectional study (CSBrS-001). Ann Transl Med. 2021;9(20):1588. https://doi.org/10.21037/atm-21-5169CrossRefPubMedPubMedCentral

31.

Johnston SRD, Harbeck N, Hegg R, Toi M, Martin M, Shao ZM, Zhang QY, Martinez Rodriguez JL, Campone M, Hamilton E, Sohn J, Guarneri V, Okada M, Boyle F, Neven P, Cortés J, Huober J, Wardley A, Tolaney SM, Cicin I, Smith IC, Frenzel M, Headley D, Wei R, San Antonio B, Hulstijn M, Cox J, O’Shaughnessy J. Priya Rastogi. Abemaciclib combined with endocrine therapy for the adjuvant treatment of HR+, HER2-, node-nositive, high-risk, early breast bancer (monarchE). J Clin Oncol. 2020;38(34):3987–98.CrossRefPubMedPubMedCentral

32.

Santiago RJ, Harris EE, Qin L, Hwang WT, Solin LJ. Similar long-term results of breast-conservation treatment for stage I and II invasive lobular carcinoma compared with invasive ductal carcinoma of the breast: the University of Pennsylvania experience. Cancer. 2005;103:2447–54. https://doi.org/10.1002/cncr.21071CrossRefPubMed

Title: Correlation between sentinel lymph node biopsy and non-sentinel lymph node metastasis in patients with cN0 breast carcinoma: comparison of invasive ductal carcinoma and invasive lobular carcinoma
Authors: Calogero Cipolla
Simona Lupo
Nello Grassi
Giuseppe Tutino
Martina Greco
D’Agati Eleonora
Vittorio Gebbia
Maria Rosaria Valerio
Publication date: 01-12-2024
Publisher: BioMed Central
Keywords: Metastasis
Breast Cancer
Breast Cancer
Published in: World Journal of Surgical Oncology / Issue 1/2024
Electronic ISSN: 1477-7819
DOI: https://doi.org/10.1186/s12957-024-03375-9

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Correlation between sentinel lymph node biopsy and non-sentinel lymph node metastasis in patients with cN0 breast carcinoma: comparison of invasive ductal carcinoma and invasive lobular carcinoma

Abstract

Background

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Please log in to get access to this content

Other articles of this Issue 1/2024

Feasibility of laparoscopic versus open pancreatoduodenectomy following neoadjuvant chemotherapy for borderline resectable pancreatic cancer: a retrospective cohort study

Efficacy and safety of direct oral anticoagulants versus low-molecular-weight heparin for thromboprophylaxis after cancer surgery: a systematic review and meta-analysis

Clinical impact of ampulla of Vater cancer subtype classification based on immunohistochemical staining

Immune characteristics of dedifferentiated retroperitoneal liposarcomas and the reliability of regional samples in evaluating their tumor immune microenvironments

Correction: The high-risk features and effect of postoperative radiotherapy on survival for patients with surgically treated stage IIIA-N2 non-small cell lung cancer

Predictive accuracy of boosted regression model in estimating risk of venous thromboembolism following minimally invasive radical surgery in pharmacological prophylaxis-naïve men with prostate cancer