Abstract
Background
For breast cancer patients, a false-negative rate lower than 10% can be achieved if targeted axillary dissection (TAD) is performed, which includes the excision of both biopsy-proven positive lymph nodes (BxLNs) and sentinel lymph nodes (SLNs). However, little evidence exists on the accuracy of intraoperative touch imprint cytology (ITPC) applied in TAD after neoadjuvant chemotherapy (NAC) for breast cancer patients with initial axillary metastasis. This study aimed to investigate the accuracy of ITPC in TAD after NAC.
Methods
Breast cancer patients with biopsy-confirmed nodal metastasis were prospectively enrolled in the study. After completion of NAC, all patients underwent TAD followed by axillary lymph node dissection (ALND). Then ITPC was performed to evaluate BxLNs and SLNs. The accuracy of TAD and ITPC was calculated in comparison with hematoxylin and eosin (H&E) staining of ALNs. The results of ITPC during 6 months at our center in the adjuvant setting were used for comparison .
Results
Overall, the false-negative rate of TAD was 10.8%. In a test with 92 patients, ITPC had an accuracy of 92.4%, a sensitivity of 87.9%, and a specificity of 94.9%. In the non-NAC group, ITPC showed similar accuracy (91.2%) and specificity (97.9%) but significantly lower sensitivity (68.9%; P = 0.03).
Conclusions
The use of ITPC was feasible for TAD among breast cancer patients with biopsy-confirmed axillary metastasis who were treated with NAC. All the misses in the ITPC involved patients with micrometastases or isolated tumor cells. Use of ITPC can help decrease the number of second operations for patients with residual disease in ALNs after NAC.
Similar content being viewed by others
References
Krag DN, Anderson SJ, Julian TB, et al. 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. 2010;11:927–33.
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;384:164–72.
Boughey JC, McCall LM, Ballman KV, et al. Tumor biology correlates with rates of breast-conserving surgery and pathologic complete response after neoadjuvant chemotherapy for breast cancer: findings from the ACOSOG Z1071 (Alliance) Prospective Multicenter Clinical Trial. Ann Surg. 2014;260:608–14.
Dominici LS, Negron Gonzalez VM, Buzdar AU, et al. Cytologically proven axillary lymph node metastases are eradicated in patients receiving preoperative chemotherapy with concurrent trastuzumab for HER2-positive breast cancer. Cancer. 2010;116:2884–9.
Li JW, Mo M, Yu KD, et al. ER-poor and HER2-positive: a potential subtype of breast cancer to avoid axillary dissection in node positive patients after neoadjuvant chemo-trastuzumab therapy. PLOS One. 2014;9:e114646.
Kuehn T, Bauerfeind I, Fehm T, 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.
Boughey JC, Suman VJ, Mittendorf EA, 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.
Boileau JF, Poirier B, Basik M, 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.
Boughey JC, Suman VJ, Mittendorf EA, et al. Factors affecting sentinel lymph node identification rate after neoadjuvant chemotherapy for breast cancer patients enrolled in ACOSOG Z1071 (Alliance). Ann Surg. 2015;261:547–52.
Boughey JC, Ballman KV, Le-Petross HT, et al. Identification and resection of clipped node decreases the false-negative rate of sentinel lymph node surgery in patients presenting with node-positive breast cancer (T0-T4, N1-N2) who receive neoadjuvant chemotherapy: results from ACOSOG Z1071 (Alliance). Ann Surg. 2016;263:802–7.
Caudle AS, Yang WT, Krishnamurthy S, et al. Improved axillary evaluation following neoadjuvant therapy for patients with node-positive breast cancer using selective evaluation of clipped nodes: implementation of targeted axillary dissection. J Clin Oncol. 2016;34:1072–8.
Chen JJ, Yang BL, Zhang JX, Xu WP, Shao ZM, Wu J. The evaluation and optimization of intraoperative touch imprint cytology for sentinel lymph nodes in early-stage breast cancer in China. World J Surg. 2010;34:2325–32.
Gimbergues P, Dauplat MM, Durando X, et al. Intraoperative imprint cytology examination of sentinel lymph nodes after neoadjuvant chemotherapy in breast cancer patients. Ann Surg Oncol. 2010;17:2132–7.
Komenaka IK, Torabi R, Nair G, et al. Intraoperative touch imprint and frozen section analysis of sentinel lymph nodes after neoadjuvant chemotherapy for breast cancer. Ann Surg. 2010;251:319–22.
Wolff AC, Hammond ME, Hicks DG, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. Arch Pathol Lab Med. 2014;138:241–56.
Yu KD, Liu GY, Chen CM, et al. Weekly paclitaxel/carboplatin/trastuzumab therapy improves pathologic complete remission in aggressive HER2-positive breast cancers, especially in luminal-B subtype, compared with a once-every-3-weeks schedule. Oncologist. 2013;18:511–7.
Donker M, Straver ME, Wesseling J, et al. Marking axillary lymph nodes with radioactive iodine seeds for axillary staging after neoadjuvant systemic treatment in breast cancer patients: the MARI procedure. Ann Surg. 2015;261:378–82.
Diego EJ, McAuliffe PF, Soran A, McGuire KP, Johnson RR, Bonaventura M, Ahrendt GM. Axillary staging after neoadjuvant chemotherapy for breast cancer: a pilot study combining sentinel lymph node biopsy with radioactive seed localization of pre-treatment positive axillary lymph nodes. Ann Surg Oncol. 2016;23:1549–53.
Nguyen TT, Hieken TJ, Glazebrook KN, Boughey JC. Localizing the clipped node in patients with node-positive breast cancer treated with neoadjuvant chemotherapy: early learning experience and challenges. Ann Surg Oncol. 2017;24:3011–6.
Tew K, Irwig L, Matthews A, Crowe P, Macaskill P. Meta-analysis of sentinel node imprint cytology in breast cancer. Br J Surg. 2005;92:1068–80.
Cox C, Centeno B, Dickson D, et al. Accuracy of intraoperative imprint cytology for sentinel lymph node evaluation in the treatment of breast carcinoma. Cancer. 2005;105:13–20.
Contractor K, Gohel M, Al-Salami E, et al. Intra-operative imprint cytology for assessing the sentinel node in breast cancer: results of its routine use over 8 years. Eur J Surg Oncol. 2009;35:16–20.
Giuliano AE, Ballman K, McCall L, et al. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: long-term follow-up from the American College of Surgeons Oncology Group (Alliance) ACOSOG Z0011 randomized trial. Ann Surg. 2016;264:413–20.
van der Noordaa MEM, Vrancken Peeters MTFD, Rutgers EJT. The intraoperative assessment of sentinel nodes: standards and controversies. Breast. 2017;34(Suppl 1):S64–9.
Shimazu K, Tamaki Y, Taguchi T, Tsukamoto F, Kasugai T, Noguchi S. Intraoperative frozen section analysis of sentinel lymph node in breast cancer patients treated with neoadjuvant chemotherapy. Ann Surg Oncol. 2008;15:1717–22.
Rubio IT, 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;17:235–9.
Miller AR, Thomason VE, Yeh IT, 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.
Jain P, Kumar R, Anand M, et al. Touch imprint cytology of axillary lymph nodes after neoadjuvant chemotherapy in patients with breast carcinoma. Cancer. 2003;99:346–51.
Jegaraj A, Kadambari D, Srinivasan K, Siddaraju N. Imprint cytology of axillary lymph nodes in breast carcinoma following neoadjuvant chemotherapy. Acta Cytol. 2010;54:685–91.
Aguiar PH, Pinheiro LG, Mota RM, Margotti NH, Rocha JI. Sentinel lymph node biopsy in patients with locally advanced breast cancer after neoadjuvant chemotherapy. Acta Cir Bras. 2012;27:912–6.
Elliott RM, Shenk RR, Thompson CL, Gilmore HL. Touch preparations for the intraoperative evaluation of sentinel lymph nodes after neoadjuvant therapy have high false-negative rates in patients with breast cancer. Arch Pathol Lab Med. 2014;138:814–8.
Acknowledgments
The authors thank all participating patients and clinicians for contributing data to this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Disclosure
There are no conflicts of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Fig. S1
Touch imprints of a positive biopsied lymph node during (A) targeted axillary dissection (TAD) and (B) sentinel lymph node biopsy (SLNB) alone (hematoxylin and eosin staining) (TIFF 6093 kb)
Rights and permissions
About this article
Cite this article
Wu, S., Wang, Y., Zhang, N. et al. Intraoperative Touch Imprint Cytology in Targeted Axillary Dissection After Neoadjuvant Chemotherapy for Breast Cancer Patients with Initial Axillary Metastasis. Ann Surg Oncol 25, 3150–3157 (2018). https://doi.org/10.1245/s10434-018-6548-9
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1245/s10434-018-6548-9