Annals of Surgical Oncology

, Volume 24, Issue 11, pp 3124–3132 | Cite as

Locoregional Recurrence Following Breast Cancer Surgery in the Trastuzumab Era: A Systematic Review by Subtype

  • Andrew McGuire
  • Aoife J. Lowery
  • Malcolm R. Kell
  • Michael J. Kerin
  • Karl J. Sweeney
Breast Oncology
  • 115 Downloads

Abstract

Introduction

Increasing evidence suggests that molecular subtype influences locoregional recurrence (LRR) of breast cancer. Previous systematic reviews that evaluated the quantitative influence of subtype on LRR predated the use of Trastuzumab. This study assessed the impact of subtype on LRR in a contemporary treatment era.

Methods

A comprehensive search for all published studies assessing LRR according to breast cancer subtype was performed. Only studies with patients treated with Trastuzumab were included. Relevant data were extracted from each study for systematic review. Primary outcome was LRR related to breast cancer subtype.

Results

In total, 11,219 patients were identified from seven studies. Overall LRR rate was 3.44%. The lowest LRR rates were in luminal A (1.7%), and the highest rates were in triple-negative (7.4%) subtypes. There were significantly lower risks of LRR in patients with luminal A subtype compared with luminal B [odds ratio (OR) 0.54, 95% confidence interval (CI) 0.38–0.76; p < 0.0004], HER2/neu-overexpressing (OR 0.32, 95% CI 0.24–0.45; p < 0.0001) and triple-negative breast cancers (OR 0.25, 95% CI 0.19–0.32; p < 0.0001). There were significant differences in LRR between the luminal B and HER2/neu-overexpressing breast cancers (OR 0.61, 95% CI 0.41–0.89; p = 0.0145). The reduced risk in HER2/neu overexpressing compared with triple-negative breast cancers approached statistical significance (OR 0.75, 95% CI 0.55–1.03; p = 0.0933).

Conclusions

Significant variations in LRR occur across breast cancer subtypes, with lowest rates in luminal cancers and highest rates in triple-negative breast cancers. Low levels of LRR highlight advances in breast cancer management in the contemporary era.

Supplementary material

10434_2017_6021_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 15 kb)
10434_2017_6021_MOESM2_ESM.pptx (67 kb)
Supplementary material 2 (PPTX 67 kb)

References

  1. 1.
    Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature 2000;406(6797):747–52.CrossRefPubMedGoogle Scholar
  2. 2.
    Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thurlimann B, Senn HJ. Strategies for subtypes—dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol. 2011;22(8):1736–47.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Dobbe E, Gurney K, Kiekow S, Lafferty JS, Kolesar JM. Gene-expression assays: new tools to individualize treatment of early-stage breast cancer. Am J Health Syst Pharm. 2008;65(1):23–8.CrossRefPubMedGoogle Scholar
  4. 4.
    Goss PE, Ingle JN, Martino S, et al. Randomized trial of letrozole following tamoxifen as extended adjuvant therapy in receptor-positive breast cancer: updated findings from NCIC CTG MA.17. J Natl Cancer Inst. 2005;97(17):1262–71.CrossRefPubMedGoogle Scholar
  5. 5.
    Piccart-Gebhart MJ, Procter M, Leyland-Jones B, et al. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med. 2005;353(16):1659–72.CrossRefPubMedGoogle Scholar
  6. 6.
    Kennecke H, Yerushalmi R, Woods R, et al. Metastatic behavior of breast cancer subtypes. J Clin Oncol. 2010;28(20):3271–7.CrossRefPubMedGoogle Scholar
  7. 7.
    Clarke M, Collins R, Darby S, et al. Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials. Lancet 2005;366(9503):2087–106.CrossRefPubMedGoogle Scholar
  8. 8.
    Lowery AJ, Kell MR, Glynn RW, Kerin MJ, Sweeney KJ. Locoregional recurrence after breast cancer surgery: a systematic review by receptor phenotype. Breast Cancer Res Treat. 2012;133(3):831–41.CrossRefPubMedGoogle Scholar
  9. 9.
    Hudis CA. Trastuzumab—mechanism of action and use in clinical practice. N Engl J Med. 2007;357(1):39–51.CrossRefPubMedGoogle Scholar
  10. 10.
    Slamon DJ, Leyland-Jones B, Shak S, et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med. 2001;344(11):783–92.CrossRefPubMedGoogle Scholar
  11. 11.
    Romond EH, Perez EA, Bryant J, et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med. 2005;353(16):1673–84.CrossRefPubMedGoogle Scholar
  12. 12.
    Perez EA, Romond EH, Suman VJ, et al. Four-year follow-up of trastuzumab plus adjuvant chemotherapy for operable human epidermal growth factor receptor 2-positive breast cancer: joint analysis of data from NCCTG N9831 and NSABP B-31. J Clin Oncol. 2011;29(25):3366–73.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Gianni L, Eiermann W, Semiglazov V, et al. Neoadjuvant chemotherapy with trastuzumab followed by adjuvant trastuzumab versus neoadjuvant chemotherapy alone, in patients with HER2-positive locally advanced breast cancer (the NOAH trial): a randomised controlled superiority trial with a parallel HER2-negative cohort. Lancet 2010;375(9712):377–84.CrossRefPubMedGoogle Scholar
  14. 14.
    Buzdar AU, Ibrahim NK, Francis D, et al. Significantly higher pathologic complete remission rate after neoadjuvant therapy with trastuzumab, paclitaxel, and epirubicin chemotherapy: results of a randomized trial in human epidermal growth factor receptor 2-positive operable breast cancer. J Clin Oncol. 2005;23(16):3676–85.CrossRefPubMedGoogle Scholar
  15. 15.
    Untch M, Rezai M, Loibl S, et al. Neoadjuvant treatment with trastuzumab in HER2-positive breast cancer: results from the GeparQuattro study. J Clin Oncol. 2010;28(12):2024–31.CrossRefPubMedGoogle Scholar
  16. 16.
    Viani GA, Afonso SL, Stefano EJ, De Fendi LI, Soares FV. Adjuvant trastuzumab in the treatment of her-2-positive early breast cancer: a meta-analysis of published randomized trials. BMC Cancer 2007;7:153.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Mazouni C, Rimareix F, Mathieu MC, et al. Outcome in breast molecular subtypes according to nodal status and surgical procedures. Am J Surg. 2013;205(6):662–7.CrossRefPubMedGoogle Scholar
  18. 18.
    Yamazaki N, Wada N, Yamauchi C, Yoneyama K. High expression of post-treatment Ki-67 status is a risk factor for locoregional recurrence following breast-conserving surgery after neoadjuvant chemotherapy. Eur J Surg Oncol. 2015;41(5):617–24.CrossRefPubMedGoogle Scholar
  19. 19.
    Mersin H, Gulben K, Berberoglu U, et al. Prognostic factors affecting postmastectomy locoregional recurrence in patients with early breast cancer: are intrinsic subtypes effective? World J Surg. 2011;35(10):2196–202.CrossRefPubMedGoogle Scholar
  20. 20.
    Kim MM, Dawood S, Allen P, et al. Hormone receptor status influences the locoregional benefit of trastuzumab in patients with nonmetastatic breast cancer. Cancer 2012;118(20):4936–43.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Shim HJ, Kim SH, Kang BJ, et al. Breast cancer recurrence according to molecular subtype. Asian Pac J Cancer Prev. 2014;15(14):5539–44.CrossRefPubMedGoogle Scholar
  22. 22.
    Lee Y, Kang E, Lee AS, et al. Outcomes and recurrence patterns according to breast cancer subtypes in Korean women. Breast Cancer Res Treat. 2015;151(1):183–90.CrossRefPubMedGoogle Scholar
  23. 23.
    Swisher SK, Vila J, Tucker SL, et al. Locoregional control according to breast cancer subtype and response to neoadjuvant chemotherapy in breast cancer patients undergoing breast-conserving therapy. Ann Surg Oncol. 2016;23(3):749–56.CrossRefPubMedGoogle Scholar
  24. 24.
    Voduc KD, Cheang MC, Tyldesley S, Gelmon K, Nielsen TO, Kennecke H. Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol. 2010;28(10):1684–91.CrossRefPubMedGoogle Scholar
  25. 25.
    Dowsett M, Cuzick J, Ingle J, et al. Meta-analysis of breast cancer outcomes in adjuvant trials of aromatase inhibitors versus tamoxifen. J Clin Oncol. 2010;28(3):509–18.CrossRefPubMedGoogle Scholar
  26. 26.
    Group EBCTC. Tamoxifen for early breast cancer: an overview of the randomised trials. Early Breast Cancer Trialists’ Collaborative Group. Lancet 1998;351(9114):1451–67.CrossRefGoogle Scholar
  27. 27.
    Cortazar P, Zhang L, Untch M, et al. Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet 2014;384(9938):164–72.CrossRefPubMedGoogle Scholar
  28. 28.
    Kiess AP, McArthur HL, Mahoney K, et al. Adjuvant trastuzumab reduces locoregional recurrence in women who receive breast-conservation therapy for lymph node-negative, human epidermal growth factor receptor 2-positive breast cancer. Cancer 2011;118(8):1982–8.CrossRefPubMedGoogle Scholar
  29. 29.
    Pivot X, Romieu G, Debled M, et al. 6 Months versus 12 months of adjuvant trastuzumab for patients with HER2-positive early breast cancer (PHARE): a randomised phase 3 trial. Lancet Oncol. 2013;14(8):741–8.CrossRefPubMedGoogle Scholar
  30. 30.
    Smith I, Procter M, Gelber RD, et al. 2-Year follow-up of trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer: a randomised controlled trial. Lancet 2007;369(9555):29–36.CrossRefPubMedGoogle Scholar
  31. 31.
    Liedtke C, Mazouni C, Hess KR, et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J Clin Oncol. 2008;26(8):1275–81.CrossRefPubMedGoogle Scholar
  32. 32.
    Carey LA, Dees EC, Sawyer L, et al. The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res. 2007;13(8):2329–34.CrossRefPubMedGoogle Scholar
  33. 33.
    Network TCGA. Comprehensive molecular portraits of human breast tumours. Nature 2012;490(7418):61–70.CrossRefGoogle Scholar
  34. 34.
    Foulkes WD, Stefansson IM, Chappuis PO, et al. Germline BRCA1 mutations and a basal epithelial phenotype in breast cancer. J Natl Cancer Inst. 2003;95(19):1482–5.CrossRefPubMedGoogle Scholar
  35. 35.
    Darby S, McGale P, Correa C, et al. Effect of radiotherapy after breast-conserving surgery on 10-year recurrence and 15-year breast cancer death: meta-analysis of individual patient data for 10,801 women in 17 randomised trials. Lancet 2011;378(9804):1707–16.CrossRefPubMedGoogle Scholar
  36. 36.
    Fisher B, Anderson S, Bryant J, et al. 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. 2002;347(16):1233–41.CrossRefPubMedGoogle Scholar
  37. 37.
    Moran MS, Schnitt SJ, Giuliano AE, et al. Society of Surgical Oncology-American Society for Radiation Oncology consensus guideline on margins for breast-conserving surgery with whole-breast irradiation in stages I and II invasive breast cancer. Ann Surg Oncol. 2014;21(3):704–16.CrossRefPubMedGoogle Scholar
  38. 38.
    Abdulkarim BS, Cuartero J, Hanson J, Deschenes J, Lesniak D, Sabri S. Increased risk of locoregional recurrence for women with T1-2N0 triple-negative breast cancer treated with modified radical mastectomy without adjuvant radiation therapy compared with breast-conserving therapy. J Clin Oncol. 2011;29(21):2852–8.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Adkins FC, Gonzalez-Angulo AM, Lei X, et al. Triple-negative breast cancer is not a contraindication for breast conservation. Ann Surg Oncol. 2011;18(11):3164–73.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Ragaz J, Olivotto IA, Spinelli JJ, et al. Locoregional radiation therapy in patients with high-risk breast cancer receiving adjuvant chemotherapy: 20-year results of the British Columbia randomized trial. J Natl Cancer Inst. 2005;97(2):116–26.CrossRefPubMedGoogle Scholar
  41. 41.
    Nielsen HM, Overgaard M, Grau C, Jensen AR, Overgaard J. Study of failure pattern among high-risk breast cancer patients with or without postmastectomy radiotherapy in addition to adjuvant systemic therapy: long-term results from the Danish Breast Cancer Cooperative Group DBCG 82 b and c randomized studies. J Clin Oncol. 2006;24(15):2268–75.CrossRefPubMedGoogle Scholar
  42. 42.
    Taylor ME, Haffty BG, Rabinovitch R, et al. ACR appropriateness criteria on postmastectomy radiotherapy: Expert Panel on Radiation Oncology-Breast. Int J Radiat Oncol Biol Phys. 2009;73(4):997–1002.CrossRefPubMedGoogle Scholar
  43. 43.
    Carlson RW, Allred DC, Anderson BO, et al. Breast cancer. Clinical practice guidelines in oncology. J Natl Compr Cancer Netw. 2009;7(2):122–92.CrossRefGoogle Scholar
  44. 44.
    Kyndi M, Sorensen FB, Knudsen H, Overgaard M, Nielsen HM, Overgaard J. 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(9):1419–26.CrossRefPubMedGoogle Scholar

Copyright information

© Society of Surgical Oncology 2017

Authors and Affiliations

  • Andrew McGuire
    • 1
  • Aoife J. Lowery
    • 1
  • Malcolm R. Kell
    • 2
  • Michael J. Kerin
    • 1
  • Karl J. Sweeney
    • 1
    • 3
  1. 1.Discipline of Surgery, School of MedicineNational University of IrelandGalwayIreland
  2. 2.Department of Surgery and Eccles Breast Screening UnitMater Misericordiae University HospitalDublinIreland
  3. 3.BreastCheck, Western UnitGalwayIreland

Personalised recommendations