A review regarding the feasibility and accuracy of a sentinel lymph node biopsy after neo-adjuvant chemotherapy for breast cancer

Background: The sentinel lymph node biopsy (SLNB) is the standard procedure to assess the lymph node status in women with early stage breast cancer. It is uncertain whether SLNB is useful after neo-adjuvant chemotherapy (NACT) given to women with locally advanced breast cancer. Materials and Methods: A literature search was conducted over a timeframe of 22 years (1994-2016). Forty-three studies evaluating the feasibility and accuracy of SLNB after NACT were identified. Results: The pooled identification rate was 88% and the pooled false negative ratio was 12%. Conclusion: SLNB could be considered as a standard procedure after NACT.

Breast cancer; Neo-adjuvant chemotherapy; Sentinel lymph node biopsy; Axillary clearance; Morbidity; SLN; Survival

[1] Tjalma W.A.: “Reimbursement for bone loss prevention is different between women with breast cancer and men with prostate cancer: time for a revision”. Facts Views Vis. Obgyn., 2015, 7, 183.

[2] Giuliano A.E., Jones R.C., Brennan M., Statman R.: “Sentinel lymphadenectomy in breast cancer”. J. Clin. Oncol., 1997, 15, 2345.

[3] Krag D., Weaver D., Ashikaga T., Moffat F., Klimberg V.S., Shriver C., et al.: “The sentinel node in breast cancer—a multicenter validation study”. N. Engl. J. Med., 1998, 339, 941.

[4] Albert A., Huyghe I., Stroobants S., Tjalma W.A.: “Three Different Locations of a Sentinel Node Highlight the Importance of Performing a Sentinel Node Biopsy in Breast Cancer Recurrence”. Breast Cancer, 2016, 10, 1.

[5] Schwartz G.F., Giuliano A.E., Veronesi U., Consensus Conference C.: “Proceedings of the consensus conference on the role of sentinel lymph node biopsy in carcinoma of the breast, April 19-22, 2001, Philadelphia, Pennsylvania”. Cancer, 2002, 94, 2542.

[6] Van Berckelaer C., Huizing M., Van Goethem M., Vervaecke A., Papadimitriou K., Verslegers I., et al.: “Preoperative ultrasound staging of the axilla make’s peroperative examination of the sentinel node redundant in breast cancer: saving tissue, time and money”. Eur. J. Obstet. Gynecol. Reprod. Biol., 2016, 206, 164.

[7] Gebruers N., Verbelen H., De Vrieze T., Vos L., Devoogdt N., Fias L., Tjalma W.: “Current and future perspectives on the evaluation, prevention and conservative management of breast cancer related lymphoedema: A best practice guideline”. Eur. J. Obstet. Gynecol. Reprod. Biol., 2017, 216, 245.

[8] Hack T.F., Cohen L., Katz J., Robson L.S., Goss P.: “Physical and psychological morbidity after axillary lymph node dissection for breast cancer”. J. Clin. Oncol., 1999, 17, 143.

[9] De Vrieze T., Coeck D., Verbelen H., Devoogdt N., Tjalma W., Gebruers N.: “Cross-cultural Psychometric Evaluation of the Dutch McGill-QoL Questionnaire for Breast Cancer Patients”. Facts Views Vis. Obgyn., 2016, 8, 205.

[10] Van Dijck S., Nelissen P., Verbelen H., Tjalma W. Gebruers N.: “The effects of physical self-management on quality of life in breast cancer patients: A systematic review”. Breast, 2016, 28, 20.

[11] Verbelen H., Gebruers N., Eeckhout F.M., Verlinden K., Tjalma W.: “Shoulder and arm morbidity in sentinel node-negative breast cancer patients: a systematic review”. Breast Cancer Res. Treat., 2014, 144, 21.

[12] Tjalma W.A.: “The contraindications for a sentinel node biopsy in breast cancer are actually indications”. Surgeon, 2015, 13, 59.

[13] Van de Wiel M., Dockx Y., Van den Wyngaert T., Stroobants S., Tjalma W.A.A., Huizing M.T.: “Neoadjuvant systemic therapy in breast cancer: Challenges and uncertainties”. Eur. J. Obstet. Gynecol. Reprod. Biol., 2017, 210, 144.

[14] Schwartz G.F., Hortobagyi G.N.: “Proceedings of the consensus conference on neoadjuvant chemotherapy in carcinoma of the breast, April 26-28, 2003, Philadelphia, Pennsylvania”. Cancer, 2004, 100, 2512.

[15] Carlson R.W., Allred D.C., Anderson B.O., Burstein H.J., Carter W.B., Edge S.B., et al.: “Breast cancer. Clinical practice guidelines in oncology”. J. Natl. Compr. Canc. Netw., 2009, 7, 122.

[16] Fisher B., Brown A., Mamounas E., Wieand S., Robidoux A., Margolese R.G., et al.: “Effect of preoperative chemotherapy on localregional disease in women with operable breast cancer: findings from National Surgical Adjuvant Breast and Bowel Project B-18”. J. Clin. Oncol., 1997, 15, 2483.

[17] Mamounas E.P., Brown A., Anderson S., Smith R., Julian T., Miller B., et al.: “Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from National Surgical Adjuvant Breast and Bowel Project Protocol B-27”. J. Clin. Oncol., 2005, 23, 2694.

[18] Al Mushawah F., Tan M.C., Margenthaler J.A.: “Axillary staging prior to or after neoadjuvant systemic therapy? A single institutional experience”. J. Surg. Oncol., 2010, 102, 404.

[19] Brady E.W.: “Sentinel lymph node mapping following neoadjuvant chemotherapy for breast cancer”. Breast J., 2002, 8, 97.

[20] Fernandez A., Cortes M., Benito E., Azpeitia D., Prieto L., Moreno A., et al.: “Gamma probe sentinel node localization and biopsy in breast cancer patients treated with a neoadjuvant chemotherapy scheme”. Nucl. Med. Commun., 2001, 22, 361.

[21] Hunt K.K., Yi M., Mittendorf E.A., Guerrero C., Babiera G.V., Bedrosian I., et al.: “Sentinel lymph node surgery after neoadjuvant chemotherapy is accurate and reduces the need for axillary dissection in breast cancer patients”. Ann. Surg., 2009, 250, 558.

[22] Stell V.H., Flippo-Morton T.S., James Norton H., White R.L., Jr.: “Sentinel lymph node biopsy after neo-adjuvant chemotherapy in breast cancer”. Breast J., 2011, 17, 71.

[23] Alvarado R., Yi M., Le-Petross H., Gilcrease M., Mittendorf E.A., Bedrosian I., et al.: “The role for sentinel lymph node dissection after neoadjuvant chemotherapy in patients who present with node-positive breast cancer”. Ann. Surg. Oncol., 2012, 19, 3177.

[24] Balch G.C., Mithani S.K., Richards K.R., Beauchamp R.D., Kelley M.C.: “Lymphatic mapping and sentinel lymphadenectomy after preoperative therapy for stage II and III breast cancer”. Ann. Surg. Oncol., 2003, 10, 616.

[25] Breslin T.M., Cohen L., Sahin A., Fleming J.B., Kuerer H.M., Newman L.A., et al.: “Sentinel lymph node biopsy is accurate after neoadjuvant chemotherapy for breast cancer”. J. Clin. Oncol., 2000, 18, 3480.

[26] Brown A.S., Hunt K.K., Shen J., Huo L., Babiera G.V., Ross M.I., et al.: “Histologic changes associated with false-negative sentinel lymph nodes after preoperative chemotherapy in patients with confirmed lymph node-positive breast cancer before treatment”. Cancer, 2010; 116, 2878.

[27] Haid A., Koeberle-Wuehrer R., Offner F., Jasarevic Z., Fritzsche H., Zimmermann G.: “Clinical usefulness and perspectives of sentinel node biopsy in the management of breast cancer”. Chirurg., 2003, 74, 657.

[28] Julian T.B., Dusi D., Wolmark N.: “Sentinel node biopsy after neoadjuvant chemotherapy for breast cancer”. Am. J. Surg., 2002, 184, 315.

[29] Nason K.S., Anderson B.O., Byrd D.R., Dunnwald L.K., Eary J.F., Mankoff D.A., et al.: “Increased false negative sentinel node biopsy rates after preoperative chemotherapy for invasive breast carcinoma”. Cancer, 2000, 89, 2187.

[30] Papa M.Z., Zippel D., Kaufman B., Shimon-Paluch S., Yosepovich A., Oberman B., et al.: “Timing of sentinel lymph node biopsy in patients receiving neoadjuvant chemotherapy for breast cancer”. J. Surg. Oncol., 2008, 98, 403.

[31] Schwartz G.F., Tannebaum J.E., Jernigan A.M., Palazzo J.P.: “Axillary sentinel lymph node biopsy after neoadjuvant chemotherapy for carcinoma of the breast”. Cancer, 2010, 116, 1243.

[32] Shen J., Gilcrease M.Z., Babiera G.V., Ross M.I., Meric-Bernstam F., Feig B.W., et al.: “Feasibility and accuracy of sentinel lymph node biopsy after preoperative chemotherapy in breast cancer patients with documented axillary metastases”. Cancer, 2007, 109, 1255.

[33] Tafra L., Verbanac K.M., Lannin D.R.: “Preoperative chemotherapy and sentinel lymphadenectomy for breast cancer”. Am. J. Surg., 2001, 182, 312.

[34] Thomas S., Prakash A., Goyal V., Popli M.B., Agarwal S., Choudhury M.: “Evaluation of sentinel node biopsy in locally advanced breast cancer patients who become clinically node-negative after neoadjuvant chemotherapy: a preliminary study”. Int. J. Breast Cancer, 2011, 2011, 870263.

[35] Takahashi M., Jinno H., Hayashida T., Sakata M., Asakura K., Kitagawa Y.: “Correlation between clinical nodal status and sentinel lymph node biopsy false negative rate after neoadjuvant chemotherapy”. world J. Surg., 2012, 36, 2847.

[36] Stearns V., Ewing C.A., Slack R., Penannen M.F., Hayes D.F., Tsangaris T.N.: “Sentinel lymphadenectomy after neoadjuvant chemotherapy for breast cancer may reliably represent the axilla except for inflammatory breast cancer”. Ann. Surg. Oncol., 2002, 9, 235.

[37] Lang J.E., Esserman L.J., Ewing C.A., Rugo H.S., Lane K.T., Leong S.P., et al.: “Accuracy of selective sentinel lymphadenectomy after neoadjuvant chemotherapy: effect of clinical node status at presentation”. J. Am. Coll. Surg., 2004, 199, 856.

[38] Kinoshita T.: “Sentinel lymph node biopsy is feasible for breast cancer patients after neoadjuvant chemotherapy”. Breast Cancer, 2007, 14, 10.

[39] Tausch C., Konstantiniuk P., Kugler F., Reitsamer R., Roka S., Postlberger S., et al.: “Sentinel lymph node biopsy after preoperative chemotherapy for breast cancer: findings from the Austrian Sentinel Node Study Group”. Ann. Surg. Oncol., 2008, 15, 3378.

[40] Hino M., Sano M., Sato N., Homma K.: “Sentinel lymph node biopsy after neoadjuvant chemotherapy in a patient with operable breast cancer”. Surg. Today, 2008, 38, 585.

[41] Gimbergues P., Abrial C., Durando X., Le Bouedec G., Cachin F., Penault-Llorca F., et al.: “Sentinel lymph node biopsy after neoadjuvant chemotherapy is accurate in breast cancer patients with a clinically negative axillary nodal status at presentation”. Ann. Surg. Oncol., 2008, 15, 1316.

[42] Ozmen V., Unal E.S., Muslumanoglu M.E., Igci A., Canbay E., Ozcinar B., et al.: “Axillary sentinel node biopsy after neoadjuvant chemotherapy”. Eur. J. Surg. Oncol., 2010, 36, 23.

[43] Rubio I.T., Aznar F., Lirola J., Peg V., Xercavins J.: “Intraoperative assessment of sentinel lymph nodes after neoadjuvant chemotherapy in patients with breast cancer”. Ann. Surg. Oncol., 2010, 17, 235.

[44] Classe J.M., Bordes V., Campion L., Mignotte H., Dravet F., Leveque J., et al.: “Sentinel lymph node biopsy after neoadjuvant chemotherapy for advanced breast cancer: results of Ganglion Sentinelle et Chimiotherapie Neoadjuvante, a French prospective multicentric study”. J. Clin. Oncol., 2009, 27, 726.

[45] Pecha V., Kolarik D., Kozevnikova R., Hovorkova K., Hrabetova P., Halaska M., et al.: “Sentinel lymph node biopsy in breast cancer patients treated with neoadjuvant chemotherapy”. Cancer, 2011, 117, 4606.

[46] Zhang G.C., Liao N., Guo Z.B., Qian X.K., Ren C.Y., Yao M., et al.: “Accuracy and axilla sparing potentials of sentinel lymph node biopsy with methylene blue alone performed before versus after neoadjuvant chemotherapy in breast cancer: a single institution experience”. Clin. Transl. Oncol., 2013, 15, 79.

[47] Lee S., Kim E.Y., Kang S.H., Kim S.W., Kim S.K., Kang K.W., et al.: “Sentinel node identification rate, but not accuracy, is significantly decreased after pre-operative chemotherapy in axillary nodepositive breast cancer patients”. Breast Cancer Res. Treat., 2007, 102, 283.

[48] Kuehn T., Bauerfeind I., Fehm T., Fleige B., Hausschild M., Helms G., et al.: “Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study”. Lancet Oncol., 2013, 14, 609.

[49] Kang S.H., Kang J.H., Choi E.A., Lee E.S.: “Sentinel lymph node biopsy after neoadjuvant chemotherapy”. Breast Cancer, 2004, 11, 233.

[50] Hunt K.K., Ballman K.V., McCall L.M., Boughey J.C., Mittendorf E.A., Cox C.E., et al.: “Factors associated with local-regional recurrence after a negative sentinel node dissection: results of the ACOSOG Z0010 trial”. Ann. Surg., 2012, 256, 428.

[51] Boughey J.C., Suman V.J., Mittendorf E.A., Ahrendt G.M., Wilke L.G., Taback B., et al.: “Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial”. JAMA, 2013, 310, 1455.

[52] Park S., Lee J.E., Paik H.J., Ryu J.M., Bae S.Y., Lee S.K., et al.: “Feasibility and Prognostic Effect of Sentinel Lymph Node Biopsy After Neoadjuvant Chemotherapy in Cytology-Proven, Node-Positive Breast Cancer”. Clin. Breast Cancer, 2017, 17, e19.

[53] Boileau J.F., Poirier B., Basik M., Holloway C.M., Gaboury L., Sideris L., et al.: “Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study”. J. Clin. Oncol., 2015, 33, 258.

[54] Goldhirsch A., Wood W.C., Coates A.S., Gelber R.D., Thurlimann B., Senn H.J., et al.: “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, 1736.

[55] AGO, DGS, SGS, ÖGS, Panelists, Executive Board Members, et al.: “German, Austrian and Swiss consensus conference on the diagnosis and local treatment of the axilla in breast cancer”. Eur. J. Cancer, 2013, 49, 2277.

[56] Galimberti V., Cole B.F., Zurrida S., Viale G., Luini A., Veronesi P., 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.

[57] Giuliano A.E., McCall L., Beitsch P., Whitworth P.W., Blumencranz P., Leitch A.M., 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.

[58] Kim T., Giuliano A.E., Lyman G.H.: “Lymphatic mapping and sentinel lymph node biopsy in early-stage breast carcinoma: a metaanalysis”. Cancer, 2006, 106, 4.

[59] Fraile M., Rull M., Julian F.J., Fuste F., Barnadas A., Llatjos M., et al.: “Sentinel node biopsy as a practical alternative to axillary lymph node dissection in breast cancer patients: an approach to its validity”. Ann Oncol., 2000, 11, 701.

[60] Miltenburg D.M., Miller C., Karamlou T.B., Brunicardi F.C.: “Metaanalysis of sentinel lymph node biopsy in breast cancer”. J. Surg. Res., 1999, 84, 138.

[61] Khan A., Sabel M.S., Nees A., Diehl K.M., Cimmino V.M., Kleer C.G., et al.: “Comprehensive axillary evaluation in neoadjuvant chemotherapy patients with ultrasonography and sentinel lymph node biopsy”. Ann. Surg. Oncol., 2005, 12, 697.

[62] Newman E.A., Sabel M.S., Nees A.V., Schott A., Diehl K.M., Cimmino V.M., et al.: “Sentinel lymph node biopsy performed after neoadjuvant chemotherapy is accurate in patients with documented node-positive breast cancer at presentation”. Ann. Surg. Oncol., 2007, 14, 2946.

[63] Canavese G., Dozin B., Vecchio C., Tomei D., Villa G., Carli F., et al.: “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. Oncol., 2011, 37, 688.

[64] Chintamani, Tandon M., Mishra A., Agarwal U., Saxena S.: “Sentinel lymph node biopsy using dye alone method is reliable and accurate even after neo-adjuvant chemotherapy in locally advanced breast cancer—a prospective study”. world J. Surg. Oncol., 2011, 9, 19.

[65] Takei H., Yoshida T., Kurosumi M., Inoue K., Matsumoto H., Hayashi Y., et al.: “Sentinel lymph node biopsy after neoadjuvant chemotherapy predicts pathological axillary lymph node status in breast cancer patients with clinically positive axillary lymph nodes at presentation”. Int. J. Clin. Oncol., 2013, 18, 547.

[66] Rebollo-Aguirre A.C., Gallego-Peinado M., Sanchez-Sanchez R., Pastor-Pons E., Garcia-Garcia J., Chamorro-Santos C.E., et al.: “Sentinel lymph node biopsy after neoadjuvant chemotherapy in patients with operable breast cancer and positive axillary nodes at initial diagnosis”. Rev. Esp. Med. Nucl. Imagen. Mol., 2013, 32, 240.

[67] Yagata H., Yamauchi H., Tsugawa K., Hayashi N., Yoshida A., Kajiura Y., et al.: “Sentinel node biopsy after neoadjuvant chemotherapy in cytologically proven node-positive breast cancer”. Clin. Breast Cancer, 2013, 13, 471.

[68] Park S., Park J.M., Cho J.H., Park H.S., Kim S.I., Park B.W.: “Sentinel lymph node biopsy after neoadjuvant chemotherapy in patients with cytologically proven node-positive breast cancer at diagnosis”. Ann. Surg. Oncol., 2013, 20, 2858.

[69] Han A., Moon H.G., Kim J., Ahn S.K., Park I.A., Han W., et al.: “Reliability of sentinel lymph node biopsy after neoadjuvant chemotherapy in breast cancer patients”. J. Breast Cancer, 2013, 16, 378.

[70] Kim J.Y., Kim M.K., Lee J.E., Jung Y., Bae S.Y., Lee S.K., et al.: “Sentinel lymph node biopsy alone after neoadjuvant chemotherapy in patients with initial cytology-proven axillary node metastasis”. J. Breast Cancer, 2015, 18, 22.

[71] Yu Y., Cui N., Li H.Y., Wu Y.M., Xu L., Fang M., et al.: “Sentinel lymph node biopsy after neoadjuvant chemotherapy for breast cancer: retrospective comparative evaluation of clinically axillary lymph node positive and negative patients, including those with axillary lymph node metastases confirmed by fine needle aspiration”. BMC Cancer, 2016, 16, 808.

[72] Enokido K., Watanabe C., Nakamura S., Ogiya A., Osako T., Akiyama F., et al.: “Sentinel Lymph Node Biopsy After Neoadjuvant Chemotherapy in Patients With an Initial Diagnosis of CytologyProven Lymph Node-Positive Breast Cancer”. Clin. Breast Cancer, 2016, 16, 299.

[73] Carlson R.W., McCormick B.: “Update: NCCN breast cancer Clinical Practice Guidelines”. J. Natl. Compr. Canc. Netw., 2005, 3, S7.

[74] Bader A.A., Tamussino K.F.: “Sentinel nodes might not reflect nodal status after neoadjuvant chemotherapy”. Am. J. Surg., 2007, 194, 135.

[75] Tanaka Y., Maeda H., Ogawa Y., Nishioka A., Itoh S., Kubota K., et al.: “Sentinel node biopsy in breast cancer patients treated with neoadjuvant chemotherapy”. Oncol. Rep., 2006, 15, 927.