This article offers a review of the literature on current surgical management of the axilla in breast cancer. This includes the decision-making process involved in clinically node-negative patients versus clinically node-positive patients, with discussion of the indications for sentinel lymph node biopsy versus axillary dissection. It also examines the surgical axillary management of patients who receive neoadjuvant chemotherapy. This article will help update practicing surgeons on the evolving research and guidelines for the management of breast cancer axillary disease.
Get full access to this article
View all access options for this article.
References
1.
CarterC.L., AllenC., HensonD.E.Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases.Cancer1989; 63: 181–7.
2.
BeenkenS.W., UristM.M., ZhangY.Axillary lymph node status, but not tumor size, predicts locoregional recurrence and overall survival after mastectomy for breast cancer.Ann Surg2003; 237: 732–8, discussion 738–9.
3.
GiulianoA.E., JonesR.C., BrennanM.Sentinel lymphadenectomy in breast cancer.J Clin Oncol1997; 15: 2345–50.
4.
KragD.N., AndersonS.J., JulianT.B.Technical outcomes of sentinel-lymph-node resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial.Lancet Oncol2007; 8: 881–8.
5.
GiulianoA.E., McCallL., BeitschP.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 Surg2010; 252(3): 426–32, discussion 432–23.
6.
BougheyJ.C., SumanV.J., MittendorfE.A.Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial.JAMA2013; 310: 1455–61.
7.
KuehnT., BauerfeindI., FehmT.Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study.Lancet Oncol2013; 14: 609–18.
8.
CaudleA.S., CuppJ.A., KuererH.M.Management of axillary disease.Surg Oncol Clin N Am2014; 23: 473–86.
Edge SB, American Joint Committee on Cancer.AJCC Cancer Staging Manual, 7th ed.New York: Springer, 2010.
11.
SacreR.A.Clinical evaluation of axillar lymph nodes compared to surgical and pathological findings.Eur J Surg Oncol1986; 12: 169–73.
12.
KrishnamurthyS.Current applications and future prospects of fine-needle aspiration biopsy of locoregional lymph nodes in the management of breast cancer.Cancer2009; 117: 451–62.
13.
GouldE.A., WinshipT., PhilbinP.H.Observations on a “sentinel node” in cancer of the parotid.Cancer1960; 13: 77–8.
14.
CabanasR.M.An approach for the treatment of penile carcinoma.Cancer1977; 39: 456–66.
15.
RobinsonD.S., SampleW.F., FeeH.J.Regional lymphatic drainage in primary malignant melanoma of the trunk determined by colloidal gold scanning.Surg Forum1977; 28: 147–8.
16.
GiulianoA.E., KirganD.M., GuentherJ.M.Lymphatic mapping and sentinel lymphadenectomy for breast cancer.Ann Surg1994; 220: 391–8, discussion 398–401.
17.
McMastersK.M., TuttleT.M., CarlsonD.J.Sentinel lymph node biopsy for breast cancer: a suitable alternative to routine axillary dissection in multi-institutional practice when optimal technique is used.J Clin Oncol2000; 18: 2560–6.
18.
MartinR.C.II, EdwardsM.J., WongS.L.Practical guidelines for optimal gamma probe detection of sentinel lymph nodes in breast cancer: results of a multi-institutional study. For the University of Louisville Breast Cancer Study Group.Surgery2000; 128: 139–44.
19.
WongS.L., EdwardsM.J., ChaoC.Sentinel lymph node biopsy for breast cancer: impact of the number of sentinel nodes removed on the false-negative rate.J Am Coll Surg2001; 192: 684–9, discussion 689–91.
20.
GoyalA., NewcombeR.G., ChhabraA.Factors affecting failed localisation and false-negative rates of sentinel node biopsy in breast cancer—results of the ALMANAC validation phase.Breast Cancer Res Treat2006; 99: 203–8.
21.
LymanG.H., TeminS., EdgeS.B.Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology clinical practice guideline update.J Clin Oncol2014; 32: 1365–83.
22.
KragD.N., AndersonS.J., JulianT.B.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 Oncol2010; 11: 927–33.
23.
HarlowS.P., KragD.N., JulianT.B.Prerandomization Surgical Training for the National Surgical Adjuvant Breast and Bowel Project (NSABP) B-32 trial: a randomized phase III clinical trial to compare sentinel node resection to conventional axillary dissection in clinically node-negative breast cancer.Ann Surg2005; 241: 48–54.
24.
WeaverD.L., AshikagaT., KragD.N.Effect of occult metastases on survival in node-negative breast cancer.N Engl J Med2011; 364: 412–21.
25.
FleissigA., FallowfieldL.J., LangridgeC.I.Post-operative 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 Treat2006; 95: 279–93.
26.
ManselR.E., FallowfieldL., KissinM.Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC trial.J Natl Cancer Inst2006; 98: 599–609.
27.
ZavagnoG., Del BiancoP., KoussisH.Clinical impact of false-negative sentinel lymph nodes in breast cancer.Eur J Surg Oncol2008; 34: 620–5.
28.
Del BiancoP., ZavagnoG., BurelliP.Morbidity comparison of sentinel lymph node biopsy versus conventional axillary lymph node dissection for breast cancer patients: results of the sentinella–GIVOM Italian randomised clinical trial.Eur J Surg Oncol2008; 34: 508–13.
29.
ZavagnoG., De SalvoG.L., ScalcoG.A Randomized clinical trial on sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer: results of the Sentinella/GIVOM trial.Ann Surg2008; 247: 207–13.
30.
CanaveseG., CatturichA., VecchioC.Sentinel node biopsy compared with complete axillary dissection for staging early breast cancer with clinically negative lymph nodes: results of randomized trial.Ann Oncol2009; 20: 1001–7.
31.
GillP.G.Sentinel lymph node biopsy versus axillary clearance in operable breast cancer: the RACS SNAC trial, a multicenter randomized trial of the Royal Australian College of Surgeons (RACS) Section of Breast Surgery, in collaboration with the National Health and Medical Research Council Clinical Trials Center.Ann Surg Oncol2004; 11(Suppl): 216S–21S.
32.
SmithM.J., GillP.G., WetzigN.Comparing patients’ and clinicians’ assessment of outcomes in a randomised trial of sentinel node biopsy for breast cancer (the RACS SNAC trial).Breast Cancer Res Treat2009; 117: 99–109.
33.
UngO.A.Australasian experience and trials in sentinel lymph node biopsy: the RACS SNAC trial.Asian J Surg2004; 27: 284–90.
34.
BochnerM.A., KolliasJ., GillP.G.Implication of intraoperative sentinel node imprint cytology for consent in the SNAC Trial.ANZ J Surg2004; 74: 105–7.
35.
VeronesiU., PaganelliG., VialeG.Sentinel-lymph-node biopsy as a staging procedure in breast cancer: update of a randomised controlled study.Lancet Oncol2006; 7: 983–90.
36.
VeronesiU., VialeG., PaganelliG.Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study.Ann Surg2010; 251: 595–600.
37.
PurushothamA.D., UpponiS., KlevesathM.B.Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial.J Clin Oncol2005; 23: 4312–21.
38.
AshikagaT., KragD.N., LandS.R.Morbidity results from the NSABP B-32 trial comparing sentinel lymph node dissection versus axillary dissection.J Surg Oncol2010; 102: 111–8.
39.
GiulianoA.E., HawesD., BallmanK.V.Association of occult metastases in sentinel lymph nodes and bone marrow with survival among women with early-stage invasive breast cancer.JAMA2011; 306: 385–93.
40.
KimbroughC.W., McMastersK.M., QuilloA.Occult metastases in node-negative breast cancer: a surveillance, epidemiology, and end results-based analysis.Surgery2015; 158: 494–500.
41.
ChenS.L., HoehneF.M., GiulianoA.E.The prognostic significance of micrometastases in breast cancer: a SEER population-based analysis.Ann Surg Oncol2007; 14: 3378–84.
MittendorfE.A., SahinA.A., TuckerS.L.Lymphovascular invasion and lobular histology are associated with increased incidence of isolated tumor cells in sentinel lymph nodes from early-stage breast cancer patients.Ann Surg Oncol2008; 15: 3369–77.
44.
GiulianoA.E., HuntK.K., BallmanK.V.Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial.JAMA2011; 305: 569–75.
45.
GalimbertiV., ColeB.F., ZurridaS.Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23-01): a phase 3 randomised controlled trial.Lancet Oncol2013; 14: 297–305.
46.
DonkerM., van TienhovenG., StraverM.E.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 Oncol2014; 15: 1303–10.
47.
MorrowM.Rethinking the local therapy of breast cancer: integration of biology and anatomy.Ann Surg Oncol2015; 22: 3168–73.
HoussamiN., TurnerR.M.Staging the axilla in women with breast cancer: the utility of preoperative ultrasound-guided needle biopsy.Cancer Biol Med2014; 11: 69–77.
50.
HarrisJ.R., LippmanM.E., MorrowM.Diseases of the Breast, 5th ed.Philadelphia, PA: Wolters Kluwer/Lippincott Williams & Wilkins Health, 2014.
51.
MieogJ.S., van der HageJ.A., van de VeldeC.J.Neoadjuvant chemotherapy for operable breast cancer.Br J Surg2007; 94: 1189–200.
52.
MauriD., PavlidisN., IoannidisJ.P.Neoadjuvant versus adjuvant systemic treatment in breast cancer: a meta-analysis.J Natl Cancer Inst2005; 97: 188–94.
53.
FisherB., BrownA., MamounasE.Effect of pre-operative chemotherapy on local-regional disease in women with operable breast cancer: findings from National Surgical Adjuvant Breast and Bowel Project B-18.J Clin Oncol1997; 15: 2483–93.
54.
KuererH.M., SahinA.A., HuntK.K.Incidence and impact of documented eradication of breast cancer axillary lymph node metastases before surgery in patients treated with neo-adjuvant chemotherapy.Ann Surg1999; 230: 72–8.
55.
KingT.A., MorrowM.Surgical issues in patients with breast cancer receiving neoadjuvant chemotherapy.Nat Rev Clin Oncol2015; 12: 335–43.
56.
MamounasE.P., BrownA., AndersonS.Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from National Surgical Adjuvant Breast and Bowel Project Protocol B-27.J Clin Oncol2005; 23: 2694–702.
57.
HuntK.K., YiM., MittendorfE.A.Sentinel lymph node surgery after neoadjuvant chemotherapy is accurate and reduces the need for axillary dissection in breast cancer patients.Ann Surg2009; 250: 558–66.
58.
MamounasE.P., AndersonS.J., DignamJ.J.Predictors of locoregional recurrence after neoadjuvant chemotherapy: results from combined analysis of National Surgical Adjuvant Breast and Bowel Project B-18 and B-27.J Clin Oncol2012; 30: 3960–6.
59.
LeeS., KimE.Y., KangS.H.Sentinel node identification rate, but not accuracy, is significantly decreased after pre-operative chemotherapy in axillary node-positive breast cancer patients.Breast Cancer Res Treat2007; 102: 283–8.
60.
PatelN.A., PiperG., PatelJ.A.Accurate axillary nodal staging can be achieved after neoadjuvant therapy for locally advanced breast cancer.Am Surg2004; 70: 696–9, discussion 699–700.
61.
CanaveseG., DozinB., VecchioC.Accuracy of sentinel lymph node biopsy after neo-adjuvant chemotherapy in patients with locally advanced breast cancer and clinically positive axillary nodes.Eur J Surg Oncol2011; 37: 688–94.
62.
BoileauJ.F., PoirierB., BasikM.Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study.J Clin Oncol2015; 33: 258–64.
63.
Comparison of Axillary Lymph Node Dissection With Axillary Radiation for Patients With Node-Positive Breast Cancer Treated With Chemotherapy. Available at: https://clinicaltrials.gov/ct2/show/NCT01901094. Accessed October 13, 2015.
64.
Standard or Comprehensive Radiation Therapy in Treating Patients With Early-Stage Breast Cancer Previously Treated With Chemotherapy and Surgery. Available at: https://clinicaltrials.gov/ct2/show/NCT01872975. Accessed October 13, 2015.
65.
VirnigB.A., TuttleT.M., ShamliyanT.Ductal carcinoma in situ of the breast: a systematic review of incidence, treatment, and outcomes.J Natl Cancer Inst2010; 102: 170–8.
66.
VerkooijenH.M., PeetersP.H., BuskensE.Diagnostic accuracy of large-core needle biopsy for nonpalpable breast disease: a meta-analysis.Br J Cancer2000; 82: 1017–21.
67.
PataniN., CutuliB., MokbelK.Current management of DCIS: a review.Breast Cancer Res Treat2008; 111: 1–10.
68.
SilversteinM.J., RosserR.J., GiersonE.D.Axillary lymph node dissection for intraductal breast carcinoma—is it indicated?Cancer1987; 59: 1819–24.
69.
McMastersK.M., ChaoC., WongS.L.Sentinel lymph node biopsy in patients with ductal carcinoma in situ: a proposal.Cancer2002; 95: 15–20.
70.
LymanG.H., GiulianoA.E., SomerfieldM.R.American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer.J Clin Oncol2005; 23: 7703–20.
71.
HafftyB.G., HuntK.K., HarrisJ.R.Positive sentinel nodes without axillary dissection: implications for the radiation oncologist.J Clin Oncol2011; 29: 4479–81.
72.
WhelanT.J., AckermanI.O.I., ChapmanJ.W.NCIC-CTG MA.20: an intergroup trial of regional nodal irradiation in early breast cancer. [Abstract]. J Clin Oncol2011; 29.
73.
ClarkeM., CollinsR., DarbyS.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.Lancet2005; 366: 2087–106.
74.
ChengJ.C., ChenC.M., LiuM.C.Locoregional failure of postmastectomy patients with 1-3 positive axillary lymph nodes without adjuvant radiotherapy.Int J Radiat Oncol Biol Phys2002; 52: 980–8.
