Assessment of sentinel lymph node biopsy after neoadjuvant chemotherapy for breast cancer in two subgroups: Initially node negative and node positive converted to node negative - A systemic review and meta-analysis

Alireza Shirzadi, Habibollah Mahmoodzadeh, Mostafa Qorbani, Alireza Shirzadi, Habibollah Mahmoodzadeh, Mostafa Qorbani

Abstract

Background: Neoadjuvant chemotherapy (NAC) is increasingly used to treat patients with breast cancer, but the reliability of sentinel lymph node biopsy (SLNB) following chemotherapy is in doubt. In this meta-analysis, we aimed to evaluate studies that examine the results of SLNB after NAC to assess identification rate (IR) and false-negative rate (FNR).

Materials and methods: Systemic searches were performed in the PubMed, ISI Web of Sciences, Scopus, and Cochrane databases from January 1, 2000, to November 30, 2016, for studies of SLNB after NAC for breast cancer and followed by axillary lymph node (LN) dissection in two subgroups: initially node negative and node positive converted to node negative. Two reviewers independently review quality of included studies. A random-effects model was used to pool IR and FNR with 95% confidence intervals (CI), and heterogeneity among studies was assessed by I 2 and Q-test.

Results: A total of 23 studies with 1521 patients in the initially node-negative subgroup and 13 studies with 1088 patients in the node-positive converted to node-negative subgroup, were included in this meta-analysis with IR and FNR of 94% (95% CI: 92-96) and 7% (95% CI: 5-9) in the initially node-negative subgroup and 89% (95% CI: 85-94) and 13% (95% CI: 7-18) in the node-positive converted to node-negative subgroup, respectively.

Conclusion: Our meta-analysis showed acceptable IR and FNR in initially node-negative group and it seems feasible in these patients, but these parameters did not reach to predefined value in node-positive converted to node-negative group, and thus, it is not recommended in these patients.

Keywords: Breast cancer; meta-analysis; neoadjuvant systemic therapy; sentinel lymph node biopsy.

Conflict of interest statement

There are no conflicts of interest.

Figures

Figure 1
Figure 1
Flow diagram of literature search
Figure 2
Figure 2
(a) Forest plot of the identification rate in initially node-negative patients, (b) forest plot of the false-negative rate in initially node-negative patients
Figure 3
Figure 3
(a) Forest plot of the identification rate in node-positive converted to node-negative patients, (b) forest plot of the false-negative rate in node-positive converted to node-negative patients

References

    1. Patten DK, Zacharioudakis KE, Chauhan H, Cleator SJ, Hadjiminas DJ. Sentinel lymph node biopsy after neo-adjuvant chemotherapy in patients with breast cancer: Are the current false negative rates acceptable? Breast. 2015;24:318–20.
    1. Benson JR, Jatoi I. Sentinel lymph node biopsy and neoadjuvant chemotherapy in breast cancer patients. Future Oncol. 2014;10:577–86.
    1. Shimazu K, Noguchi S. Sentinel lymph node biopsy before versus after neoadjuvant chemotherapy for breast cancer. Surg Today. 2011;41:311–6.
    1. Kang SH, Kang JH, Choi EA, Lee ES. Sentinel lymph node biopsy after neoadjuvant chemotherapy. Breast Cancer. 2004;11:233–41.
    1. Rubio IT. Sentinel lymph node biopsy after neoadjuvant treatment in breast cancer: Work in progress. Eur J Surg Oncol. 2016;42:326–32.
    1. Cao XS, Li HJ, Cong BB, Sun X, Qiu PF, Liu YB, et al. Axillary and internal mammary sentinel lymph node biopsy in breast cancer after neoadjuvant chemotherapy. Oncotarget. 2016;7:74074–81.
    1. Andreis D, Bonardi S, Allevi G, Aguggini S, Gussago F, Milani M, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with T2 to T4, N0 and N1 breast cancer. Breast. 2016;29:55–61.
    1. Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: A revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155:529–36.
    1. Fletcher J. What is heterogeneity and is it important? BMJ. 2007;334:94–6.
    1. Talebi M. Study of publication bias in meta-analysis using trim and fill method. Int Res J Appl Basic Sci. 2013;4:31–6.
    1. Nason KS, Anderson BO, Byrd DR, Dunnwald LK, Eary JF, Mankoff DA, et al. Increased false negative sentinel node biopsy rates after preoperative chemotherapy for invasive breast carcinoma. Cancer. 2000;89:2187–94.
    1. Tafra L, Verbanac KM, Lannin DR. Preoperative chemotherapy and sentinel lymphadenectomy for breast cancer. Am J Surg. 2001;182:312–5.
    1. Miller AR, Thomason VE, Yeh IT, Alrahwan A, Sharkey FE, Stauffer J, et al. Analysis of sentinel lymph node mapping with immediate pathologic review in patients receiving preoperative chemotherapy for breast carcinoma. Ann Surg Oncol. 2002;9:243–7.
    1. Vigario A, Sapienza MT, Sampaio AP, Piato JR, Barros N, Barros A, et al. Primary chemotherapy effect in sentinel node detection in breast cancer. Clin Nucl Med. 2003;28:553–7.
    1. Piato JR, Barros AC, Pincerato KM, Sampaio AP, Pinotti JA. Sentinel lymph node biopsy in breast cancer after neoadjuvant chemotherapy. A pilot study. Eur J Surg Oncol. 2003;29:118–20.
    1. Lang JE, Esserman LJ, Ewing CA, Rugo HS, Lane KT, Leong SP, et al. Accuracy of selective sentinel lymphadenectomy after neoadjuvant chemotherapy: Effect of clinical node status at presentation. J Am Coll Surg. 2004;199:856–62.
    1. 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. 2005;15:927–31.
    1. Jones JL, Zabicki K, Christian RL, Gadd MA, Hughes KS, Lesnikoski BA, et al. Acomparison of sentinel node biopsy before and after neoadjuvant chemotherapy: Timing is important. Am J Surg. 2005;190:517–20.
    1. Mamounas EP, 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;23:2694–702.
    1. Yu JC, Hsu GC, Hsieh CB, Yu CP, Chao TY. Role of sentinel lymphadenectomy combined with intraoperative ultrasound in the assessment of locally advanced breast cancer after neoadjuvant chemotherapy. Ann Surg Oncol. 2007;14:174–80.
    1. Kinoshita T. Sentinel lymph node biopsy is feasible for breast cancer patients after neoadjuvant chemotherapy. Breast Cancer. 2007;14:10–5.
    1. 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;15:1316–21.
    1. Papa MZ, 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;98:403–6.
    1. Classe JM, 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;27:726–32.
    1. Hunt KK, Yi M, Mittendorf EA, Guerrero C, Babiera GV, 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;250:558–66.
    1. Cheung TT, Suen DT, Kwong A. Is sentinel lymph node biopsy after neoadjuvant chemotherapy feasible in Chinese patients with invasive breast cancers? Surg Oncol. 2009;79:719–23.
    1. 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;117:4606–16.
    1. Takahashi M, Jinno H, Hayashida T, Sakata M, Asakura K, Kitagawa Y, et al. Correlation between clinical nodal status and sentinel lymph node biopsy false negative rate after neoadjuvant chemotherapy. World J Surg. 2012;36:2847–52.
    1. Rebollo-Aguirre AC, Gallego-Peinado M, Menjón-Beltrán S, García-García J, Pastor-Pons E, Chamorro-Santos CE, et al. Sentinel lymph node biopsy in patients with operable breast cancer treated with neoadjuvant chemotherapy. Rev Esp Med Nucl Imagen Mol. 2012;31:117–23.
    1. Shigekawa T, Sugitani I, Takeuchi H, Misumi M, Nakamiya N, Sugiyama M, et al. Axillary ultrasound examination is useful for selecting patients optimally suited for sentinel lymph node biopsy after primary systemic chemotherapy. Am J Surg. 2012;204:487–93.
    1. Piñero-Madrona A, Escudero-Barea MJ, Fernández-Robayna F, Alberro-Adúriz JA, García-Fernández A, Vicente-García F, et al. Selective sentinel lymph node biopsy after neoadjuvant chemotherapy in breast cancer: Results of the GEICAM 2005-07 study. Cir Esp. 2015;93:23–9.
    1. Kida K, Ishikawa T, Yamada A, Shimizu D, Tanabe M, Sasaki T, et al. Aprospective feasibility study of sentinel node biopsy by modified indigocarmine blue dye methods after neoadjuvant chemotherapy for breast cancer. Eur J Surg Oncol. 2015;41:566–70.
    1. Ozmen V, Unal ES, Muslumanoglu ME, Igci A, Canbay E, Ozcinar B, et al. Axillary sentinel node biopsy after neoadjuvant chemotherapy. Eur J Surg Oncol. 2010;36:23–9.
    1. Thomas S, Prakash A, Goyal V, Popli MB, Agarwal S, Choudhury M, et al. 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.
    1. 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.
    1. Rebollo-Aguirre AC, Gallego-Peinado M, Sánchez-Sánchez R, Pastor-Pons E, García-García J, Chamorro-Santos CE, 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;32:240–5.
    1. 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;14:609–18.
    1. Lee HD, Ahn SG, Lee SA, Lee HM, Jeong J. Prospective evaluation of the feasibility of sentinel lymph node biopsy in breast cancer patients with negative axillary conversion after neoadjuvant chemotherapy. Cancer Res Treat. 2015;47:26–33.
    1. Yu Y, Cui N, Li HY, Wu YM, 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.
    1. Carrera D, de la Flor M, Galera J, Amillano K, Gomez M, Izquierdo V, et al. Validation of sentinel lymph node biopsy in breast cancer women N1-N2 with complete axillary response after neoadjuvant chemotherapy. Multicentre study in Tarragona. Rev Esp Med Nucl Imagen Mol. 2016;35:221–5.
    1. Geng C, Chen X, Pan X, Li J. The feasibility and accuracy of sentinel lymph node biopsy in initially clinically node-negative breast cancer after neoadjuvant chemotherapy: A Systematic review and meta-analysis. PLoS One. 2016;11:e0162605.
    1. Mocellin S, Goldin E, Marchet A, Nitti D. Sentinel node biopsy performance after neoadjuvant chemotherapy in locally advanced breast cancer: A systematic review and meta-analysis. Int J Cancer. 2016;138:472–80.
    1. van Nijnatten TJ, Schipper RJ, Lobbes MB, Nelemans PJ, Beets-Tan RG, Smidt ML, et al. The diagnostic performance of sentinel lymph node biopsy in pathologically confirmed node positive breast cancer patients after neoadjuvant systemic therapy: A systematic review and meta-analysis. Eur J Surg Oncol. 2015;41:1278–87.
    1. Fu JF, Chen HL, Yang J, Yi CH, Zheng S. Feasibility and accuracy of sentinel lymph node biopsy in clinically node-positive breast cancer after neoadjuvant chemotherapy: A meta-analysis. PLoS One. 2014;9:e105316.
    1. Fontein DB, van de Water W, Mieog JS, Liefers GJ, van de Velde CJ. Timing of the sentinel lymph node biopsy in breast cancer patients receiving neoadjuvant therapy – Recommendations for clinical guidance. Eur J Surg Oncol. 2013;39:417–24.
    1. Tan VK, Goh BK, Fook-Chong S, Khin LW, Wong WK, Yong WS, et al. The feasibility and accuracy of sentinel lymph node biopsy in clinically node-negative patients after neoadjuvant chemotherapy for breast cancer – a systematic review and meta-analysis. J Surg Oncol. 2011;104:97–103.
    1. van Deurzen CH, Vriens BE, Tjan-Heijnen VC, van der Wall E, Albregts M, van Hilligersberg R, et al. Accuracy of sentinel node biopsy after neoadjuvant chemotherapy in breast cancer patients: A systematic review. Eur J Cancer. 2009;45:3124–30.
    1. Xing Y, Foy M, Cox DD, Kuerer HM, Hunt KK, Cormier JN, et al. Meta-analysis of sentinel lymph node biopsy after preoperative chemotherapy in patients with breast cancer. Br J Surg. 2006;93:539–46.
    1. Harlow SP, Krag DN, Julian TB, Ashikaga T, Weaver DL, Feldman SA, et al. 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 Surg. 2005;241:48–54.
    1. Kim T, Giuliano AE, Lyman GH. Lymphatic mapping and sentinel lymph node biopsy in early-stage breast carcinoma: A metaanalysis. Cancer. 2006;106:4–16.
    1. Han A, Moon HG, Kim J, Ahn SK, Park IA, Han W, et al. Reliability of sentinel lymph node biopsy after neoadjuvant chemotherapy in breast cancer patients. J Breast Cancer. 2013;16:378–85.
    1. van der Heiden-van der Loo M, de Munck L, Sonke GS, van Dalen T, van Diest PJ, van den Bongard HJ, et al. Population based study on sentinel node biopsy before or after neoadjuvant chemotherapy in clinically node negative breast cancer patients: Identification rate and influence on axillary treatment. Eur J Cancer. 2015;51:915–21.
    1. Lee S, Kim EY, Kang SH, Kim SW, Kim SK, Kang KW, et al. Sentinel node identification rate, but not accuracy, is significantly decreased after pre-operative chemotherapy in axillary node-positive breast cancer patients. Breast Cancer Res Treat. 2007;102:283–8.
    1. Boughey JC, Suman VJ, Mittendorf EA, Ahrendt GM, Wilke LG, Taback B, et al. The role of sentinel lymph node surgery in patients presenting with node positive breast cancer (T0-T4, N1-2) who receive neoadjuvant chemotherapy – Results from the ACOSOG Z1071 trial. Cancer Res Suppl. 2012;72:94s.
    1. Boileau JF, Poirier B, Basik M, Holloway CM, 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;33:258–64.
    1. Boughey JC, Suman VJ, Mittendorf EA, Ahrendt GM, Wilke LG, 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;310:1455–61.
    1. Park S, Park JM, Cho JH, Park HS, Kim SI, Park BW, et al. Sentinel lymph node biopsy after neoadjuvant chemotherapy in patients with cytologically proven node-positive breast cancer at diagnosis. Ann Surg Oncol. 2013;20:2858–65.
    1. Wong SL, Edwards MJ, Chao C, Tuttle TM, Noyes RD, Carlson DJ, et al. Sentinel lymph node biopsy for breast cancer: Impact of the number of sentinel nodes removed on the false-negative rate. J Am Coll Surg. 2001;192:684–9.
    1. Lyman GH. Appropriate role for sentinel node biopsy after neoadjuvant chemotherapy in patients with early-stage breast cancer. J Clin Oncol. 2015;33:232–4.
    1. Hunt KK, Ballman KV, McCall LM, Boughey JC, Mittendorf EA, Cox CE, et al. Factors associated with local-regional recurrence after a negative sentinel node dissection: Results of the ACOSOG Z0010 trial. Ann Surg. 2012;256:428–36.

Source: PubMed

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