Advertisement

Annals of Surgical Oncology

, Volume 25, Issue 12, pp 3527–3534 | Cite as

Multidisciplinary Management of the Axilla in Patients with cT1-T2 N0 Breast Cancer Undergoing Primary Mastectomy: Results from a Prospective Single-Institution Series

  • Samantha Grossmith
  • Anvy Nguyen
  • Jiani Hu
  • Jennifer K. Plichta
  • Faina Nakhlis
  • Linda Cutone
  • Laura Dominici
  • Mehra Golshan
  • Margaret Duggan
  • Katharine Carter
  • Esther Rhei
  • Thanh Barbie
  • Katherina Calvillo
  • Suniti Nimbkar
  • Jennifer Bellon
  • Julia Wong
  • Rinaa Punglia
  • William Barry
  • Tari A. King
Breast Oncology
  • 464 Downloads

Abstract

Background

The after mapping of the axilla: radiotherapy or surgery (AMAROS) trial concluded that for patients with cT1-2 N0 breast cancer and one or two positive sentinel lymph nodes (SLNs), axillary radiotherapy (AxRT) provides equivalent locoregional control and a lower incidence of lymphedema compared with axillary lymph node dissection (ALND). The study prospectively assessed how often ALND could be replaced by AxRT in a consecutive cohort of patients undergoing mastectomy for cT1-2 N0 breast cancer.

Methods

In November 2015, our multidisciplinary group agreed to omit routine intraoperative SLN evaluation for cT1-2 N0 patients undergoing upfront mastectomy and potentially eligible for postmastectomy radiation therapy (PMRT), including those 60 years of age or younger and those older than 60 years with high-risk features. Patients with one or two positive SLNs on final pathology were reviewed to determine whether PMRT including the full axilla was an appropriate alternative to ALND.

Results

From November 2015 to December 2016, 154 patients met the study criteria, and 114 (74%) formed the final study cohort. Intraoperative SLN evaluation was omitted for 76 patients (67%). Of these patients, 20 (26%) had one or two positive SLNs, and 14 of these patients received PMRT + AxRT as an alternative to ALND. Three patients returned for ALND, and three patients were observed. On univariate analysis, tumor size, LVI, number of positive lymph nodes, and receipt of chemotherapy were associated with receipt of PMRT.

Conclusions

For the majority of patients with one or two positive SLNs, ALND was avoided in favor of PMRT + AxRT. With appropriate multidisciplinary strategies, intraoperative evaluation of the SLN and immediate ALND can be avoided for patients meeting the AMAROS criteria and eligible for PMRT.

Notes

Disclosure

There are no conflicts of interest.

Supplementary material

10434_2018_6525_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 16 kb)

References

  1. 1.
    Krag D, Weaver D, Ashikaga T, et al. The sentinel node in breast cancer: a multicenter validation study. N Engl J Med. 1998;339:941–6.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Fleissig A, Fallowfield LJ, Langridge CI, et al. Postoperative arm morbidity and quality of life: results of the ALMANAC randomised trial comparing sentinel node biopsy with standard axillary treatment in the management of patients with early breast cancer. Breast Cancer Res Treat. 2006;95:279–93.CrossRefGoogle Scholar
  3. 3.
    Krag DN, Anderson SJ, Julian TB, et al. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Veronesi U, Paganelli G, Viale G, et al. A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med. 2003;349:546–53.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Land SR, Kopec JA, Julian TB, et al. Patient-reported outcomes in sentinel node-negative adjuvant breast cancer patients receiving sentinel-node biopsy or axillary dissection: National Surgical Adjuvant Breast and Bowel Project phase III protocol B-32. J Clin Oncol. 2010;28:3929–36.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Edge SB, Niland JC, Bookman MA, Theriault RL, Ottesen R, Lepisto E, et al. Emergence of sentinel node biopsy in breast cancer as standard-of-care in academic comprehensive cancer centers. J Natl Cancer Inst. 2003;95:1514–21.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Verheuvel NC, Voogd AC, Tjan-Heijnen VC, Roumen RM. Potential impact of application of Z0011-derived criteria to omit axillary lymph node dissection in node positive breast cancer patients. Eur J Surg Oncol. 2016;42:1162–8.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Delpech Y, Bricou A, Lousquy R, et al. The exportability of the ACOSOG Z0011 criteria for omitting axillary lymph node dissection after positive sentinel lymph node biopsy findings: a multicenter study. Ann Surg Oncol. 2013;20:2556–61.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Yi M, Kuerer HM, Mittendorf EA, et al. Impact of the American college of surgeons oncology group Z0011 criteria applied to a contemporary patient population. J Am Coll Surg. 2013;216:105–13.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Giuliano AE, McCall L, Beitsch P, et al. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: the American College of Surgeons Oncology Group Z0011 randomized trial. Ann Surg. 2010;252:426–32 (discussion 32–3).PubMedPubMedCentralGoogle Scholar
  11. 11.
    Giuliano AE, Hunt KK, Ballman KV, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA. 2011;305:569–75.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Giuliano AE, Ballman KV, McCall L, 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;318:918–26.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Galimberti V, Cole BF, Zurrida S, et al. Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23-01): a phase 3 randomised controlled trial. Lancet Oncol. 2013;14:297–305.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Donker M, van Tienhoven G, Straver ME, et al. 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. 2014;15:1303–10.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Morrow M, Van Zee KJ, Patil S, et al. Axillary dissection and nodal irradiation can be avoided for most node-positive z0011-eligible breast cancers: a prospective validation study of 793 patients. Ann Surg. 2017;266:457–62.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    FitzSullivan E, Bassett RL, Kuerer HM, et al. Outcomes of sentinel lymph node-positive breast cancer patients treated with mastectomy without axillary therapy. Ann Surg Oncol. 2017;24:652–9.CrossRefGoogle Scholar
  17. 17.
    Milgrom S, Cody H, Tan L, et al. Characteristics and outcomes of sentinel node-positive breast cancer patients after total mastectomy without axillary-specific treatment. Ann Surg Oncol. 2012;19:3762–70.CrossRefGoogle Scholar
  18. 18.
    Yao K, Liederbach E, Pesce C, Wang CH, Winchester DJ. Impact of the American College of Surgeons Oncology Group Z0011 Randomized Trial on the number of axillary nodes removed for patients with early-stage breast cancer. J Am Coll Surg. 2015;221:71–81.CrossRefGoogle Scholar
  19. 19.
    Savolt A, Peley G, Polgar C, et al. Eight-year follow up result of the OTOASOR trial: the optimal treatment of the axilla: surgery or radiotherapy after positive sentinel lymph node biopsy in early-stage breast cancer: a randomized, single-centre, phase III, noninferiority trial. Eur J Surg Oncol. 2017;43:672–9.CrossRefGoogle Scholar
  20. 20.
    Moossdorff M, Nakhlis N, Hu J, et al. Management of the axilla in clinical T1-2N0 patients undergoing mastectomy: what can we learn from AMAROS? (abstract). Ann Surg Oncol. 2017;24(Suppl 1):S70 (Abstract PF5). Google Scholar
  21. 21.
    NCCN Clinical Practice Guidelines in Oncology 2017. Updated 6 April 2017. Version 2.2017: Retrieved at https://www.nccn.org/professionals/physician_gls/pdf/breast.pdf. Accessed 25 Mar 2018.
  22. 22.
    Jagsi R, Momoh AO, Qi J, et al. Impact of radiotherapy on complications and patient-reported outcomes after breast reconstruction. J Natl Cancer Inst. 2018;110:157–65.  https://doi.org/10.1093/jnci/djx148.CrossRefGoogle Scholar
  23. 23.
    Recht A, Comen EA, Fine RE, et al. Postmastectomy radiotherapy: an American Society of Clinical Oncology, American Society for Radiation Oncology, and Society of Surgical Oncology Focused Guideline Update. Pract Radiat Oncol. 2016;6:e219–34.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Recht A, Comen EA, Fine RE, et al. Postmastectomy radiotherapy: an American Society of Clinical Oncology, American Society for Radiation Oncology, and Society of Surgical Oncology Focused Guideline Update. Ann Surg Oncol. 2017;24:38–51.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Overgaard M, Nielsen HM, Overgaard J. Is the benefit of postmastectomy irradiation limited to patients with four or more positive nodes, as recommended in international consensus reports? A subgroup analysis of the DBCG 82 b&c randomized trials. Radiother Oncol. 2007;82:247–53.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Huang CJ, Hou MF, Chuang HY, et al. Comparison of clinical outcome of breast cancer patients with T1-2 tumor and one to three positive nodes with or without postmastectomy radiation therapy. Jpn J Clin Oncol. 2012;42:711–20.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Tam MM, Wu SP, Perez C, Gerber NK. The effect of post-mastectomy radiation in women with one to three positive nodes enrolled on the control arm of BCIRG-005 at ten year follow-up. Radiother Oncol. 2017;123:10–14.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Macdonald SM, Abi-Raad RF, Alm El-Din MA, et al. Chest wall radiotherapy: middle ground for treatment of patients with one to three positive lymph nodes after mastectomy. Int J Radiat Oncol Biol Phys. 2009;75:1297–303.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Huo D, Hou N, Jaskowiak N, Winchester DJ, Winchester DP, Yao K. Use of postmastectomy radiotherapy and survival rates for breast cancer patients with T1–T2 and one to three positive lymph nodes. Ann Surg Oncol. 2015;22:4295–304.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Carlson RW, Allred DC, Anderson BO, et al. Breast cancer: clinical practice guidelines in oncology. J Natl Compr Canc Netw. 2009;7:122–92.CrossRefGoogle Scholar
  31. 31.
    Kunkler IH, Canney P, van Tienhoven G, Russell NS, MRC/EORTC (BIG 2-04) SUPREMO Trial Management Group. Elucidating the role of chest wall irradiation in ‘intermediate-risk’ breast cancer: the MRC/EORTC SUPREMO trial. Clin Oncol R Coll Radiol. 2008;20:31–4.CrossRefGoogle Scholar
  32. 32.
    Thomas JS, Hanby AM, Russell N, et al. The BIG 2.04 MRC/EORTC SUPREMO Trial: pathology quality assurance of a large phase 3 randomised international clinical trial of postmastectomy radiotherapy in intermediate-risk breast cancer. Breast Cancer Res Treat. 2017;163:63–9.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Yildirim E, Berberoglu U. Local recurrence in breast carcinoma patients with T(1–2) and 1–3 positive nodes: indications for radiotherapy. Eur J Surg Oncol. 2007;33:28–32.CrossRefGoogle Scholar
  34. 34.
    Hamamoto Y, Ohsumi S, Aogi K, Shinohara S, Nakajima N, Kataoka M, et al. Are there high-risk subgroups for isolated locoregional failure in patients who had T1/2 breast cancer with one to three positive lymph nodes and received mastectomy without radiotherapy? Breast Cancer. 2014;21:177–82.CrossRefGoogle Scholar
  35. 35.
    Moo TA, McMillan R, Lee M, Stempel M, Patil S, Ho A, El-Tamer M. Selection criteria for postmastectomy radiotherapy in T1–T2 tumors with 1 to 3 positive lymph nodes. Ann Surg Oncol. 2013;20:3169–74.CrossRefGoogle Scholar
  36. 36.
    Harris EE, Freilich J, Lin HY, Chuong M, Acs G. The impact of the size of nodal metastases on recurrence risk in breast cancer patients with 1–3 positive axillary nodes after mastectomy. Int J Radiat Oncol Biol Phys. 2013;85:609–14.CrossRefGoogle Scholar
  37. 37.
    Tendulkar RD, Rehman S, Shukla ME, et al. Impact of postmastectomy radiation on locoregional recurrence in breast cancer patients with 1–3 positive lymph nodes treated with modern systemic therapy. Int J Radiat Oncol Biol Phys. 2012;83:e577–81.CrossRefGoogle Scholar
  38. 38.
    Lu C, Xu H, Chen X, Tong Z, Liu X, Jia Y. Irradiation after surgery for breast cancer patients with primary tumours and one to three positive axillary lymph nodes: yes or no? Curr Oncol. 2013;20:e585–92.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Matsunuma R, Oguchi M, Fujikane T, et al. Influence of lymphatic invasion on locoregional recurrence following mastectomy: indication for postmastectomy radiotherapy for breast cancer patients with one to three positive nodes. Int J Radiat Oncol Biol Phys. 2012;83:845–52.CrossRefGoogle Scholar
  40. 40.
    Kyndi M, Sorensen FB, Knudsen H, Overgaard M, Nielsen HM, Overgaard J, Danish Breast Cancer Cooperative Group. Estrogen receptor, progesterone receptor, HER-2, and response to postmastectomy radiotherapy in high-risk breast cancer: the Danish Breast Cancer Cooperative Group. J Clin Oncol. 2008;26:1419–26.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Cosar R, Uzal C, Tokatli F, et al. Postmastectomy irradiation in breast in breast cancer patients with T1-2 and 1–3 positive axillary lymph nodes: is there a role for radiation therapy? Radiat Oncol. 2011;6:28.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Lai SF, Chen YH, Kuo WH, et al. Locoregional recurrence risk for postmastectomy breast cancer patients with T1–2 and one to three positive lymph nodes receiving modern systemic treatment without radiotherapy. Ann Surg Oncol. 2016;23:3860–9.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Fodor J, Polgar C, Major T, Nemeth G. Locoregional failure 15 years after mastectomy in women with one to three positive axillary nodes with or without irradiation the significance of tumor size. Strahlenther Onkol. 2003;179:197–202.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Truong PT, Olivotto IA, Kader HA, Panades M, Speers CH, Berthelet E. Selecting breast cancer patients with T1–T2 tumors and one to three positive axillary nodes at high postmastectomy locoregional recurrence risk for adjuvant radiotherapy. Int J Radiat Oncol Biol Phys. 2005;61:1337–47.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Sharma R, Bedrosian I, Lucci A, et al. Present-day locoregional control in patients with T1 or T2 breast cancer with 0 and 1 to 3 positive lymph nodes after mastectomy without radiotherapy. Ann Surg Oncol. 2010;17:2899–908.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Kong M, Hong SE. Which patients might benefit from postmastectomy radiotherapy in breast cancer patients with T1–2 tumor and 1–3 axillary lymph nodes metastasis? Cancer Res Treat. 2013;45:103–11.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    He ZY, Wu SG, Zhou J, Li FY, Lin Q, Lin HX, et al. Postmastectomy radiotherapy improves disease-free survival of high risk of locoregional recurrence breast cancer patients with T1–2 and 1 to 3 positive nodes. PLoS ONE. 2015;10:e0119105.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Jwa E, Shin KH, Lim HW, et al. Identification of risk factors for locoregional recurrence in breast cancer patients with nodal stage N0 and N1: who could benefit from postmastectomy radiotherapy? PLoS ONE. 2015;10:e0145463.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Wu SG, He ZY, Li FY, Wang JJ, Guo J, Lin Q, et al. The clinical value of adjuvant radiotherapy in patients with early-stage breast cancer with 1 to 3 positive lymph nodes after mastectomy. Chin J Cancer. 2010;29:668–76.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Yin H, Qu Y, Wang X, et al. Impact of postmastectomy radiation therapy in T1–2 breast cancer patients with 1–3 positive axillary lymph nodes. Oncotarget. 2017;8:49564–73.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Straver ME, Meijnen P, van Tienhoven G, et al. Sentinel node identification rate and nodal involvement in the EORTC 10981-22023 AMAROS trial. Ann Surg Oncol. 2010;17:1854–61.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Society of Surgical Oncology 2018

Authors and Affiliations

  • Samantha Grossmith
    • 1
  • Anvy Nguyen
    • 2
  • Jiani Hu
    • 3
  • Jennifer K. Plichta
    • 2
  • Faina Nakhlis
    • 1
    • 2
  • Linda Cutone
    • 2
  • Laura Dominici
    • 1
    • 2
  • Mehra Golshan
    • 1
    • 2
  • Margaret Duggan
    • 1
    • 2
  • Katharine Carter
    • 1
    • 2
  • Esther Rhei
    • 1
    • 2
  • Thanh Barbie
    • 1
    • 2
  • Katherina Calvillo
    • 1
    • 2
  • Suniti Nimbkar
    • 1
    • 2
  • Jennifer Bellon
    • 4
  • Julia Wong
    • 4
  • Rinaa Punglia
    • 4
  • William Barry
    • 3
  • Tari A. King
    • 1
    • 2
  1. 1.Breast Surgical OncologyDana-Farber/Brigham and Women’s Cancer CenterBostonUSA
  2. 2.Department of SurgeryBrigham and Women’s HospitalBostonUSA
  3. 3.Department of Biostatistics and Computational BiologyDana-Farber Cancer InstituteBostonUSA
  4. 4.Department of Radiation OncologyDana-Farber Cancer InstituteBostonUSA

Personalised recommendations