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Sentinel and non-sentinel lymph node metastases in patients with microinvasive breast cancer: a nationwide study

  • Epidemiology
  • Published:
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Abstract

Purpose

To determine the incidence and risk factors of sentinel lymph node (SN) and non-SN metastases in patients with microinvasive breast cancer (MIBC, T1mic). This to identify MIBC patients in whom axillary staging can be safely omitted.

Methods

The Danish Breast Cancer Group database was used to identify a total of 409 women with breast cancer ≤ 1 mm who underwent sentinel lymph node biopsy (SLNB) between 2002 and 2015. After validation, 233 patients were eligible for the analysis. The incidence rates of SN and non-SN metastases were determined. The associations between clinicopathological variables and a positive SN [pN1, pN1mi, or pN0(i+)] were analyzed using univariate and multivariate designs.

Results

Of 233 patients with MIBC, only 9 (3.9%) had SN macrometastases. An additional 18 (7.7%) and 23 (9.9%) had SN micrometastases and isolated tumor cells (ITCs), respectively. Of patients with SN macrometastases, two (22.2%) had non-SN macrometastases. In the adjusted analysis, a positive SN was associated with younger age (P = 0.0001) and a positive human epidermal growth factor 2 receptor (HER2) status (P = 0.03).

Conclusions

The low incidence of SN macrometastases < 4% suggests omission of axillary staging in MIBC patients without staging at primary surgery, especially in older (≥ 50 years) HER2− patients. Still, the relatively high proportion of patients with non-SN macrometastases indicates that axillary treatment might be considered in SN positive patients, especially in younger HER2+ MIBC patients.

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References

  1. American Joint Committee on Cancer (2018) AJCC cancer staging manual, 8th edn. https://cancerstaging.org/references-tools/deskreferences/Documents/AJCC%20Breast%20Cancer%20Staging%20System.pdf. Accessed 25 Oct 2018

  2. Shatat L, Gloyeske N, Madan R, O’Neil M, Tawfik O, Fan F (2013) Microinvasive breast carcinoma carries an excellent prognosis regardless of the tumor characteristics. Hum Pathol 44(12):2684–2689. https://doi.org/10.1016/j.humpath.2013.07.010

    Article  PubMed  Google Scholar 

  3. Ko BS, Lim WS, Kim HJ, Yu JH, Lee JW, Kwan SB, Lee YM, Son BH, Gong GY, Ahn SH (2012) Risk factor for axillary lymph node metastases in microinvasive breast cancer. Ann Surg Oncol 19(1):212–216. https://doi.org/10.1245/s10434-011-1812-2

    Article  PubMed  Google Scholar 

  4. Orzalesi L, Casella D, Criscenti V, Gjondedaj U, Bianchi S, Vezzosi V, Nori J, Cecconi L, Meattini I, Livi L, Bernini M (2016) Microinvasive breast cancer: pathological parameters, cancer subtypes distribution, and correlation with axillary lymph nodes invasion. Results of a large single-institution series. Breast Cancer 23(4):640–648. https://doi.org/10.1007/s12282-015-0616-9

    Article  PubMed  Google Scholar 

  5. Hanna MG, Jaffer S, Bleiweiss IJ, Nayak A (2014) Re-evaluating the role of sentinel lymph node biopsy in microinvasive breast carcinoma. Mod Pathol 27(11):1489–1498. https://doi.org/10.1038/modpathol.2014.54

    Article  CAS  PubMed  Google Scholar 

  6. Bianchi S, Vezzosi V (2008) Microinvasive carcinoma of the breast. Pathol Oncol Res 14(2):105–111. https://doi.org/10.1007/s12253-008-9054-8

    Article  PubMed  Google Scholar 

  7. National Comprehensive Cancer Network—Clinical Practice Guidelines in Oncology (2018) https://www.nccn.org/professionals/physician_gls/pdf/breast.pdf. Accessed 20 Nov 2018

  8. Lyons JM III, Stempel M, Van Zee KJ, Cody HS III (2012) Axillary node staging for microinvasive breast cancer: is it justified? Ann Surg Oncol 19(11):3416–3421. https://doi.org/10.1245/s10434-012-2376-5

    Article  PubMed  Google Scholar 

  9. Gartner R, Jensen MB, Kronborg L, Ewertz M, Kehlet H, Kroman N (2010) Self-reported arm-lymphedema and functional impairment after breast cancer treatment—a nationwide study of prevalence and associated factors. Breast 19(6):506–515. https://doi.org/10.1016/j.breast.2010.05.015

    Article  PubMed  Google Scholar 

  10. Gartner R, Jensen MB, Nielsen J, Ewertz M, Kroman N, Kehlet H (2009) Prevalence of and factors associated with persistent pain following breast cancer surgery. JAMA 302(18):1985–1992. https://doi.org/10.1001/jama.2009.1568

    Article  PubMed  Google Scholar 

  11. Jensen MB, Laenkholm AV, Offersen BV, Christiansen P, Kroman N, Mouridsen HT, Ejlertsen B (2018) The clinical database and implementation of treatment guidelines by the Danish Breast Cancer Cooperative Group in 2007–2016. Acta Oncol 57(1):13–18. https://doi.org/10.1080/0284186X.2017.1404638

    Article  PubMed  Google Scholar 

  12. Danish Breast Cancer Group—Anvendelse af sentinel node biopsy (2013) DBCG. http://dbcg.dk/PDF%20Filer/Kap_12_Anvendelse_af_sentinel_node_06.02.13.pdf. Accessed 23 Oct 2018

  13. Gojon H, Fawunmi D, Valachis A (2014) Sentinel lymph node biopsy in patients with microinvasive breast cancer: a systematic review and meta-analysis. Eur J Surg Oncol 40(1):5–11. https://doi.org/10.1016/j.ejso.2013.10.020

    Article  CAS  PubMed  Google Scholar 

  14. Lillemoe TJ, Tsai ML, Swenson KK, Susnik B, Krueger J, Harris K, Rueth N, Grimm E, Leach JW (2018) Clinicopathologic analysis of a large series of microinvasive breast cancers. Breast J. https://doi.org/10.1111/tbj.13001

    Article  PubMed  Google Scholar 

  15. Matsen CB, Hirsch A, Eaton A, Stempel M, Heerdt A, Van Zee KJ, Cody HS III, Morrow M, Plitas G (2014) Extent of microinvasion in ductal carcinoma in situ is not associated with sentinel lymph node metastases. Ann Surg Oncol 21(10):3330–3335. https://doi.org/10.1245/s10434-014-3920-2

    Article  PubMed  PubMed Central  Google Scholar 

  16. Meretoja TJ, Heikkila PS, Salmenkivi K, Leidenius MH (2012) Outcome of patients with ductal carcinoma in situ and sentinel node biopsy. Ann Surg Oncol 19(7):2345–2351. https://doi.org/10.1245/s10434-012-2287-5

    Article  CAS  PubMed  Google Scholar 

  17. Katz A, Gage I, Evans S, Shaffer M, Fleury T, Smith FP, Flax R, Drogula C, Petrucci P, Magnant C (2006) Sentinel lymph node positivity of patients with ductal carcinoma in situ or microinvasive breast cancer. Am J Surg 191(6):761–766. https://doi.org/10.1016/j.amjsurg.2006.01.019

    Article  PubMed  Google Scholar 

  18. Pimiento JM, Lee MC, Esposito NN, Kiluk JV, Khakpour N, Carter WB, Han G, Laronga C (2011) Role of axillary staging in women diagnosed with ductal carcinoma in situ with microinvasion. J Oncol Pract 7(5):309–313. https://doi.org/10.1200/JOP.2010.000096

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kapoor NS, Shamonki J, Sim MS, Chung CT, Giuliano AE (2013) Impact of multifocality and lymph node metastasis on the prognosis and management of microinvasive breast cancer. Ann Surg Oncol 20(8):2576–2581. https://doi.org/10.1245/s10434-013-2924-7

    Article  PubMed  Google Scholar 

  20. Zavagno G, Belardinelli V, Marconato R, Carcoforo P, Franchini Z, Scalco G, Burelli P, Pietrarota P, Mencarelli R, Marconato G, Nitti D (2007) Sentinel lymph node metastasis from mammary ductal carcinoma in situ with microinvasion. Breast 16(2):146–151. https://doi.org/10.1016/j.breast.2006.08.002

    Article  PubMed  Google Scholar 

  21. 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 (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(12):1303–1310. https://doi.org/10.1016/S1470-2045(14)70460-7

    Article  PubMed  PubMed Central  Google Scholar 

  22. Kim M, Kim HJ, Chung YR, Kang E, Kim EK, Kim SH, Kim YJ, Kim JH, Kim IA, Park SY (2018) Microinvasive carcinoma versus ductal carcinoma in situ: a comparison of clinicopathological features and clinical outcomes. J Breast Cancer 21(2):197–205. https://doi.org/10.4048/jbc.2018.21.2.197

    Article  PubMed  PubMed Central  Google Scholar 

  23. DBCG (2017) Kvalitetsindikatorrapport for Brystkræft. DBCG. http://dbcg.dk/PDF%20Filer/aarsrapport_2017_final.pdf. Accessed 10 Dec 2018

  24. Leonard GD, Swain SM (2004) Ductal carcinoma in situ, complexities and challenges. J Natl Cancer Inst 96(12):906–920

    Article  PubMed  Google Scholar 

  25. Sopik V, Sun P, Narod SA (2018) Impact of microinvasion on breast cancer mortality in women with ductal carcinoma in situ. Breast Cancer Res Treat 167(3):787–795. https://doi.org/10.1007/s10549-017-4572-2

    Article  PubMed  Google Scholar 

  26. Karlsson E, Sandelin K, Appelgren J, Zhou W, Jirstrom K, Bergh J, Warnberg F (2014) Clonal alteration of breast cancer receptors between primary ductal carcinoma in situ (DCIS) and corresponding local events. Eur J Cancer 50(3):517–524. https://doi.org/10.1016/j.ejca.2013.10.020

    Article  CAS  PubMed  Google Scholar 

  27. Fortunato L, Santoni M, Drago S, Gucciardo G, Farina M, Cesarini C, Cabassi A, Tirelli C, Terribile D, Grassi GB, De Fazio S, Vitelli CE, Rome Breast Cancer Study G (2008) Sentinel lymph node biopsy in women with pT1a or “microinvasive” breast cancer. Breast 17(4):395–400. https://doi.org/10.1016/j.breast.2008.03.003

    Article  PubMed  Google Scholar 

  28. Guth AA, Mercado C, Roses DF, Darvishian F, Singh B, Cangiarella JF (2008) Microinvasive breast cancer and the role of sentinel node biopsy: an institutional experience and review of the literature. Breast J 14(4):335–339. https://doi.org/10.1111/j.1524-4741.2008.00594.x

    Article  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the Danish Cancer Society (Knæk Cancer-midlerne), Denmark (Grant Number R130-A8152-15-S38), and by the Research Fund of Rigshospitalet, (Copenhagen University Hospital), Denmark (Grant Number E-22335-01).

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Authors and Affiliations

  1. Department of Breast Surgery, Rigshospitalet/Herlev-Gentofte Hospital, Copenhagen University Hospital, Blegdamsvej 9, 2100, Copenhagen, Denmark

    Emil Villiam Holm-Rasmussen, Niels Kroman & Tove Filtenborg Tvedskov

  2. Danish Breast Cancer Group, Copenhagen University Hospital, Blegdamsvej 9, 2100, Copenhagen, Denmark

    Maj-Britt Jensen

  3. Department of Pathology, Herlev Hospital, Copenhagen University Hospital, Herlev Ringvej 75, 2730, Herlev, Denmark

    Eva Balslev

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  1. Emil Villiam Holm-Rasmussen
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Corresponding author

Correspondence to Emil Villiam Holm-Rasmussen.

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Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

The register-based study was approved by the Data Protection Agency (J. No. RH-2015-262) and the Danish Patient Safety Authority (J. No. 3-3013-1443/1/). Approvals from Ethical Committees are not needed for registry-based research in Denmark.

Informed consent

The Danish Breast Cancer Group administering the Danish Breast Cancer Database is approved by the National Health Data Authorities (J. No. 14/915974.). The Central Denmark Region holds permission to collect, store, and process data in the Danish Breast Cancer Database on all persons diagnosed with cancer in Denmark without obtaining individual consent (J. No. KPU-2001-04-2001-54-0277). In Denmark, informed consent is not required for register-based research that does not involve contact with study participants or biological samples.

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Holm-Rasmussen, E.V., Jensen, MB., Balslev, E. et al. Sentinel and non-sentinel lymph node metastases in patients with microinvasive breast cancer: a nationwide study. Breast Cancer Res Treat 175, 713–719 (2019). https://doi.org/10.1007/s10549-019-05200-4

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  • DOI: https://doi.org/10.1007/s10549-019-05200-4

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