Abstract
Sentinel lymph node biopsy (SLNB) has been recommended as the standard performance for negative sentinel lymph node (SLN) patients without axillary lymph node dissection (ALND) in the surgical management of early breast cancer; however, the efficiency of SLNB for patients with positive SLNs is still unclear. We performed this meta-analysis to compare the effectiveness and safety of SLNB with ALND. Randomized controlled trials (RCTs) comparing SLNB with ALND in early breast cancer were identified in Pubmed, Embase, and The Cochrane Library. Overall survival (OS), disease-free survival (DFS), regional lymph node recurrence, postoperative morbidity, and quality of life (QOL) between the two groups were assessed by using the methods provided by the Cochrane Handbook for Systematic Reviews of Interventions. Eight well-designed RCTs (total 8,560 patients; 4,301 for SLNB and 4,259 for ALND) were included. Meta-analysis showed that there was no statistical difference in OS (HR = 1.07, 95% CI: 0.90–1.27), DFS (HR = 1.00, 95% CI: 0.88–1.14), and regional lymph node recurrence (OR = 1.65, 95% CI: 0.77–3.56) between SLNB and ALND group, whether for SLN (+) subgroup or for SLN (−) subgroup. However, SLNB results in a significant reduction of postoperative morbidity and improved QOL. In conclusion, SLNB can be recommended as preferred care for SLN-negative patients and selected patients with SLN-micrometastasis. Despite this, ALND remains the standard management in breast cancer patients with SLN-macrometastasis.
Similar content being viewed by others
References
Coughlin SS, Ekwueme DU (2009) Breast cancer as a global health concern. Cancer Epidemiol 33(5):315–318
Samphao S, Eremin JM, El-Sheemy M, Eremin O (2008) Management of the axilla in women with breast cancer: current clinical practice and a new selective targeted approach. Ann Surg Oncol 15(5):1282–1296
Huston TL, Simmons RM (2005) Locally recurrent breast cancer after conservation therapy. Am J Surg 189(2):229–235
Roses DF, Brooks AD, Harris MN, Shapiro RL, Mitnick J (1999) Complications of level I and II axillary dissection in the treatment of carcinoma of the breast. Ann Surg 230(2):194–201
Schrenk P, Rieger R, Shamiyeh A, Wayand W (2000) Morbidity following sentinel lymph node biopsy versus axillary lymph node dissection for patients with breast carcinoma. Cancer 88(3):608–614
Kuehn T, Bembenek A, Decker T, Munz DL, Sautter-Bihl ML, Untch M, Wallwiener D (2005) A concept for the clinical implementation of sentinel lymph node biopsy in patients with breast carcinoma with special regard to quality assurance. Cancer 103(3):451–461
Veronesi U, Galimberti V, Mariani L, Gatti G, Paganelli G, Viale G, Zurrida S, Veronesi P, Intra M, Gennari R, Rita Vento A, Luini A, Tullii M, Bassani G, Rotmensz N (2005) Sentinel node biopsy in breast cancer: early results in 953 patients with negative sentinel node biopsy and no axillary dissection. Eur J Cancer 41(2):231–237
Haid A, Köberle-Wührer R, Knauer M, Burtscher J, Fritzsche H, Peschina W, Jasarevic Z, Ammann M, Hergan K, Sturn H, Zimmermann G (2002) Morbidity of breast cancer patients following complete axillary dissection or sentinel node biopsy only: a comparative evaluation. Breast Cancer Res Treat 73(1):31–36
Langer I, Guller U, Berclaz G, Koechli OR, Schaer G, Fehr MK, Hess T, Oertli D, Bronz L, Schnarwyler B, Wight E, Uehlinger U, Infanger E, Burger D, Zuber M (2007) Morbidity of sentinel lymph node biopsy (SLN) alone versus SLN and completion axillary lymph node dissection after breast cancer surgery: a prospective Swiss multicenter study on 659 patients. Ann Surg 245(3):452–461
Dabakuyo TS, Fraisse J, Causeret S, Gouy S, Padeano MM, Loustalo C, Cuisenier J, Sauzedde JM, Smail M, Combier JP, Chevillote P, Rosburger C, Boulet S, Arveux P, Bonnetain F (2009) A multicenter cohort study to compare quality of life in breast cancer patients according to sentinel lymph node biopsy or axillary lymph node dissection. Ann Oncol 20(8):1352–1361
Konstantiniuk P, Schrenk P, Reitsamer R, Koeberle-Wuehrer R, Tausch C, Roka S, Riedl O, Poestlberger S, Hecke D, Janauer M, Haid A (2007) A nonrandomized follow-up comparison between standard axillary node dissection and sentinel node biopsy in breast cancer. Breast 16(5):520–526
Abdessalam SF, Zervos EE, Prasad M, Farrar WB, Yee LD, Walker MJ, Carson WB, Burak WE Jr (2001) Predictors of positive axillary lymph nodes after sentinel lymph node biopsy in breast cancer. Am J Surg 182(4):316–320
Jeruss JS, Winchester DJ, Sener SF, Brinkmann EM, Bilimoria MM, Barrera E Jr, Alwawi E, Nickolov A, Schermerhorn GM, Winchester DJ (2005) Axillary recurrence after sentinel node biopsy. Ann Surg Oncol 12(1):34–40
Rouzier R, Extra JM, Klijanienko J, Falcou MC, Asselain B, Vincent-Salomon A, Vielh P, Bourstyn E (2002) Incidence and prognostic significance of complete axillary downstaging after primary chemotherapy in breast cancer patients with T1 to T3 tumors and cytologically proven axillary metastatic lymph nodes. J Clin Oncol 20(5):1304–1310
Menes TS, Tartter PI, Mizrachi H, Constantino J, Estabrook A, Smith SR (2005) Breast cancer patients with pN0(i+) and pN1(mi) sentinel nodes have high rate of nonsentinel node metastases. J Am Coll Surg 200(3):323–327
Noguchi M (2008) Avoidance of axillary lymph node dissection in selected patients with node-positive breast cancer. Eur J Surg Oncol 34(2):129–134
Higgins JPT, Green S, editors (2011) Cochrane handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]. The Cochrane Collaboration. http://www.cochrane-handbook.org. Accessed 29 March 2011
Moher D, Cook DJ, Eastwood S, Olkin I, Rennie D, Stroup DF (1999) Improving the quality of reports of meta-analyses of randomised controlled trials: the QUOROM statement. Quality of reporting of meta-analyses. Lancet 354(9193):1896–1900
Parmar MKB, Torri V, Stewart L (1998) Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med 17(24):2815–2834
Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR (2007) Practical methods for incorporating summary time-to-event data into meta-analysis. Trials 8: Article Number 16
Canavese G, Catturich A, Vecchio C, Tomei D, Gipponi M, Villa G, Carli F, Bruzzi P, Dozin B (2009) Sentinel node biopsy compared with complete axillary dissection for staging early breast cancer with clinically negative lymph nodes: results of randomized trial. Ann Oncol 20(6):1001–1007
Purushotham AD, Upponi S, Klevesath MB, Bobrow L, Millar K, Myles JP, Duffy SW (2005) Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol 23(19):4312–4321
Veronesi U, Viale G, Paganelli G, Zurrida S, Luini A, Galimberti V, Veronesi P, Intra M, Maisonneuve P, Zucca F, Gatti G, Mazzarol G, De Cicco C, Vezzoli D (2010) Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study. Ann Surg 251(4):595–600
Veronesi U, Paganelli G, Viale G, Luini A, Zurrida S, Galimberti V, Intra M, Veronesi P, Maisonneuve P, Gatti G, Mazzarol G, De Cicco C, Manfredi G, Fernández JR (2006) Sentinel-lymph-node biopsy as a staging procedure in breast cancer: update of a randomised controlled study. Lancet Oncol 7(12):983–990
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 (2003) A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 349(6):546–553
Fleissig A, Fallowfield LJ, Langridge CI, Johnson L, Newcombe RG, Dixon JM, Kissin M, Mansel RE (2006) 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 Treat 95(3):279–293
Mansel RE, Fallowfield L, Kissin M, Goyal A, Newcombe RG, Dixon JM, Yiangou C, Horgan K, Bundred N, Monypenny I, England D, Sibbering M, Abdullah TI, Barr L, Chetty U, Sinnett DH, Fleissig A, Clarke D, Ell PJ (2006) Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC trial. J Natl Cancer Inst 98(9):599–609
Del Bianco P, Zavagno G, Burelli P, Scalco G, Barutta L, Carraro P, Pietrarota P, Meneghini G, Morbin T, Tacchetti G, Pecoraro P, Belardinelli V, De Salvo GL (2008) 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 Oncol 34(5):508–513
Zavagno G, De Salvo GL, Scalco G, Bozza F, Barutta L, Del Bianco P, Renier M, Racano C, Carraro P, Nitti D (2008) A randomized clinical trial on sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer: results of the sentinella/GIVOM trial. Ann Surg 247(2):207–213
Ashikaga T, Krag DN, Land SR, Julian TB, Anderson SJ, Brown AM, Skelly JM, Harlow SP, Weaver DL, Mamounas EP, Costantino JP, Wolmark N (2010) Morbidity results from the NSABP B-32 trial comparing sentinel lymph node dissection versus axillary dissection. J Surg Oncol 102(2):111–118
Land SR, Kopec JA, Julian TB, Brown AM, Anderson SJ, Krag DN, Christian NJ, Costantino JP, Wolmark N, Ganz PA (2010) 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 28(25):3929–3936
Krag DN, Ashikaga T, Harlow SP, Skelly JM, Julian TB, Brown AM, Weaver DL, Wolmark N (2009) Surgeon training, protocol compliance, and technical outcomes from breast cancer sentinel lymph node randomized trial. J Natl Cancer Inst 101(19):1356–1362
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 HMC, Wolmark N (2010) 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 11(10):927–933
Smith MJ, Gill PG, Wetzig N, Sourjina T, Gebski V, Ung O, Campbell I, Kollias J, Coskinas X, MacPhee A, Young L, Simes RJ, Stockler MR (2009) 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 Treat 117(1):99–109
Gill G (2009) Sentinel-lymph-node-based management or routine axillary clearance? One-year outcomes of sentinel node biopsy versus axillary clearance (SNAC): a randomized controlled surgical trial. Ann Surg Oncol 16(2):266–275
Giuliano AE, McCall L, Beitsch P, Whitworth PW, Blumencranz P, Leitch AM, Saha S, Hunt KK, Morrow M, Ballman K (2010) 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 252(3):426–432
Lucci A, McCall LM, Beitsch PD, Whitworth PW, Reintgen DS, Blumencranz PW, Leitch AM, Saha S, Hunt KK, Giuliano AE (2007) Surgical complications associated with sentinel lymph node dissection (SLND) plus axillary lymph node dissection compared with SLND alone in the American college of surgeons oncology group trial Z0011. J Clin Oncol 25(24):3657–3663
Giuliano AE, Hunt KK, Ballman KV, Beitsch PD, Whitworth PW, Blumencranz PW, Leitch AM, Saha S, McCall LM, Morrow M (2011) Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 305(6):569–575
Pater JL, Parulekar W (2006) Sentinel lymph node biopsy in early breast cancer: has its time come? J Natl Cancer Inst 98(9):568–569
Rivers A, Hansen N (2007) Axillary management after sentinel lymph node biopsy in breast cancer patients. Surg Clin N Am 87(2):365–377
Querci Della Rovere G, Benson JR (2006) A critique of the sentinel node concept. Breast 15(6):693–697
Krag D, Weaver D, Ashikaga T, Moffat F, Klimberg VS, Shriver C, Feldman S, Kusminsky R, Gadd M, Kuhn J, Harlow S, Beitsch P, Whitworth P Jr, Foster R Jr, Dowlatshahi K (1998) The sentinel node in breast cancer. A multicenter validation study. N Engl J Med 339(14):941–946
Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Ashikaga T, Weaver DL, Miller BJ, Jalovec LM, Frazier TG, Noyes RD, Robidoux A, Scarth HM, Mammolito DM, McCready DR, Mamounas EP, Costantino JP, Wolmark N (2007) 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 Oncol 8(10):881–888
Zavagno G, Del Bianco P, Koussis H, Artioli G, Carraro P, De Salvo GL, Mencarelli R, Belardinelli V, Marconato G, Nitti D (2008) Clinical impact of false-negative sentinel lymph nodes in breast cancer. Eur J Surg Oncol 34(6):620–625
Stratmann SL, McCarty TM, Kuhn JA (1999) Radiation safety with breast sentinel node biopsy. Am J Surg 178(6):454–457
Rutgers EJ (2005) Guidelines to assure quality in breast cancer surgery. Eur J Surg Oncol 31(6):568–576
Hirche C, Murawa D, Mohr Z, Kneif S, Hünerbein M (2010) ICG fluorescence-guided sentinel node biopsy for axillary nodal staging in breast cancer. Breast Cancer Res Treat 121(2):373–378
Fant JS, Grant MD, Knox SM, Livingston SA, Ridl K, Jones RC, Kuhn JA (2003) Preliminary outcome analysis in patients with breast cancer and a positive sentinel lymph node who declined axillary dissection. Ann Surg Oncol 10(2):126–130
Paik S, Tang G, Shak S, Kim C, Baker J, Kim W, Cronin M, Baehner FL, Watson D, Bryant J, Costantino JP, Geyer CE Jr, Wickerham DL, Wolmark N (2006) Gene expression and benefit of chemotherapy in women with node-negative, estrogen receptor-positive breast cancer. J Clin Oncol 24(23):3726–3734
Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100(7):3983–3988
Degnim AC, Griffith KA, Sabel MS, Hayes DF, Cimmino VM, Diehl KM, Lucas PC, Snyder ML, Chang AE, Newman LA (2003) Clinicopathologic features of metastasis in nonsentinel lymph nodes of breast carcinoma patients: a metaanalysis. Cancer 98(11):2307–2315
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wang, Z., Wu, LC. & Chen, JQ. Sentinel lymph node biopsy compared with axillary lymph node dissection in early breast cancer: a meta-analysis. Breast Cancer Res Treat 129, 675–689 (2011). https://doi.org/10.1007/s10549-011-1665-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10549-011-1665-1