Advertisement

A Model Incorporating Axillary Tail Position on Mammography for Preoperative Prediction of Non-sentinel Lymph Node Metastasis in Patients with Initial cN+ Breast Cancer after Neoadjuvant Chemotherapy

  • Author Footnotes
    # Teng Zhu, Xiaocheng Lin and Tingfeng Zhang contributed equally to this study.
    Teng Zhu
    Footnotes
    # Teng Zhu, Xiaocheng Lin and Tingfeng Zhang contributed equally to this study.
    Affiliations
    The Second School of Clinical Medicine, Southern Medical University, Guangzhou, China

    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China
    Search for articles by this author
  • Author Footnotes
    # Teng Zhu, Xiaocheng Lin and Tingfeng Zhang contributed equally to this study.
    Xiaocheng Lin
    Footnotes
    # Teng Zhu, Xiaocheng Lin and Tingfeng Zhang contributed equally to this study.
    Affiliations
    Department of Ultrasound, Guangzhou Women and Children's Medical Center, Guangzhou, China
    Search for articles by this author
  • Author Footnotes
    # Teng Zhu, Xiaocheng Lin and Tingfeng Zhang contributed equally to this study.
    Tingfeng Zhang
    Footnotes
    # Teng Zhu, Xiaocheng Lin and Tingfeng Zhang contributed equally to this study.
    Affiliations
    The Second School of Clinical Medicine, Southern Medical University, Guangzhou, China

    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China
    Search for articles by this author
  • Weiping Li
    Affiliations
    The Second School of Clinical Medicine, Southern Medical University, Guangzhou, China

    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China
    Search for articles by this author
  • Hongfei Gao
    Affiliations
    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China
    Search for articles by this author
  • Ciqiu Yang
    Affiliations
    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China
    Search for articles by this author
  • Fei Ji
    Affiliations
    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China
    Search for articles by this author
  • Yi Zhang
    Affiliations
    The Second School of Clinical Medicine, Southern Medical University, Guangzhou, China

    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China
    Search for articles by this author
  • Junsheng Zhang
    Affiliations
    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China

    Diagnosis & Treatment Center of Breast Diseases ,Shantou University Medical College, Shantou, Guangdong, China
    Search for articles by this author
  • Weijun Pan
    Affiliations
    The Second School of Clinical Medicine, Southern Medical University, Guangzhou, China

    The First School of Clinical Medicine, Southern Medical University, Guangzhou, China
    Search for articles by this author
  • Xiaosheng Zhuang
    Affiliations
    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China

    Diagnosis & Treatment Center of Breast Diseases ,Shantou University Medical College, Shantou, Guangdong, China
    Search for articles by this author
  • Bo Shen
    Affiliations
    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China

    Diagnosis & Treatment Center of Breast Diseases ,Shantou University Medical College, Shantou, Guangdong, China
    Search for articles by this author
  • Yuanqi Chen
    Affiliations
    The Second School of Clinical Medicine, Southern Medical University, Guangzhou, China

    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China
    Search for articles by this author
  • Kun Wang
    Correspondence
    Address correspondence to: K.W.
    Affiliations
    The Second School of Clinical Medicine, Southern Medical University, Guangzhou, China

    Department of Breast Cancer, Cancer Center, Guangdong Provincial People's Hospital, Guangdong Academy of Medical Sciences, No. 123 Huifu West Road, Guangzhou, 510080, China
    Search for articles by this author
  • Author Footnotes
    # Teng Zhu, Xiaocheng Lin and Tingfeng Zhang contributed equally to this study.
Published:April 30, 2022DOI:https://doi.org/10.1016/j.acra.2022.03.012

      Rationale and Objectives

      This study aimed to develop a model incorporating axillary tail position on mammography (AT) for the prediction of non-sentinel Lymph Node (NSLN) metastasis in patients with initial clinical node positivity (cN+).

      Methods and Materials

      The study reviewed a total of 257 patients with cN+ breast cancer who underwent both sentinel lymph node biopsy (SLNB) and axillary lymph node dissection (ALND) following neoadjuvant chemotherapy (NAC). A logistic regression model was developed based on these factors and the results of post-NAC AT and axillary ultrasound (AUS).

      Results

      Four clinical factors with p<0.1 in the univariate analysis, including ycT0(odds ratio [OR]: 4.84, 95% confidence interval [CI]: 2.13-11.91, p<0.001), clinical stage before NAC (OR: 2.68, 95%CI: 1.15-6.58, p=0.025), estrogen receptor (ER) expression (OR: 3.29, 95%CI: 1.39-8.39, p=0.009), and HER2 status (OR: 0.21, 95%CI: 0.08-0.50, p=0.001), were independent predictors of NSLN metastases. The clinical model based on the above four factors resulted in the area under the curve (AUC) of 0.82(95%CI: 0.76‐0.88) in the training set and 0.83(95% CI: 0.74‐0.92) in the validation set. The results of post-NAC AUS and AT were added to the clinical model to construct a clinical imaging model for the prediction of NSLN metastasis with AUC of 0.87(95%CI: 0.81‐0.93) in the training set and 0.89(95%CI: 0.82‐0.96) in the validation set.

      Conclusions

      The study incorporated the results of post-NAC AT and AUS with other clinal factors to develop a model to predict NSLN metastasis in patients with initial cN+ before surgery. This model performed excellently, allowing physicians to select patients for whom unnecessary ALND could be avoided after NAC.

      Key Word

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Academic Radiology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Gralow J.R.
        • Burstein H.J.
        • Wood W.
        • et al.
        Preoperative therapy in invasive breast cancer: pathologic assessment and systemic therapy issues in operable disease.
        J Clin Oncol. 2008; 26: 814-819https://doi.org/10.1200/JCO.2007.15.3510
        • Killelea B.K.
        • Yang V.Q.
        • Mougalian S.
        • et al.
        Neoadjuvant chemotherapy for breast cancer increases the rate of breast conservation: results from the national cancer database.
        J Am Coll Surg. 2015; 220: 1063-1069https://doi.org/10.1016/j.jamcollsurg.2015.02.011
        • Giuliano A.E.
        • Ballman K.V
        • McCall L.
        • et al.
        Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: the ACOSOG Z0011 (Alliance) randomized clinical trial.
        JAMA. 2017; 318: 918-926https://doi.org/10.1001/jama.2017.11470
        • Galimberti V.
        • Cole B.F.
        • Viale G.
        • et al.
        Axillary dissection versus no axillary dissection in patients with breast cancer and sentinel-node micrometastases (IBCSG 23-01): 10-year follow-up of a randomised, controlled phase 3 trial.
        Lancet. Oncol. 2018; 19: 1385-1393https://doi.org/10.1016/S1470-2045(18)30380-2
        • Krag D.N.
        • Anderson S.J.
        • Julian T.B.
        • 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: 927-933https://doi.org/10.1016/S1470-2045(10)70207-2
        • Boughey J.C.
        • Suman V.J.
        • Mittendorf E.A.
        • 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: 1455-1461https://doi.org/10.1001/jama.2013.278932
        • 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: 609-618https://doi.org/10.1016/S1470-2045(13)70166-9
        • Classe J.-M.
        • Bordes V.
        • Campion L.
        • 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: 726-732https://doi.org/10.1200/JCO.2008.18.3228
        • Alvarado R.
        • Yi M.
        • Le-Petross H.
        • 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: 3177-3184https://doi.org/10.1245/s10434-012-2484-2
        • Boileau J.-F.
        • 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: 258-264https://doi.org/10.1200/JCO.2014.55.7827
        • Ryu J.M.
        • Lee S.K.
        • Kim J.Y.
        • et al.
        Predictive factors for nonsentinel lymph node metastasis in patients with positive sentinel lymph nodes after neoadjuvant chemotherapy: nomogram for predicting nonsentinel lymph node metastasis.
        Clin Breast Cancer. 2017; 17: 550-558https://doi.org/10.1016/j.clbc.2017.03.014
        • Yang Y.
        • He Y.
        • Fan Z.
        • et al.
        A new model to predict risk of nonsentinel lymph node status in Chinese sentinel lymph node-positive patients after neoadjuvant chemotherapy.
        Breast J. 2018; 24: 883-888https://doi.org/10.1111/tbj.13065
        • Le-Petross H.T.
        • McCall L.M.
        • Hunt K.K.
        • et al.
        Axillary ultrasound identifies residual nodal disease after chemotherapy: results from the american college of surgeons oncology group z1071 trial (alliance).
        AJR. Am J Roentgenol. 2018; 210: 669-676https://doi.org/10.2214/AJR.17.18295
        • Tan H.
        • Wu Y.
        • Bao F.
        • et al.
        Mammography-based radiomics nomogram: a potential biomarker to predict axillary lymph node metastasis in breast cancer.
        Br J Radiol. 2020; 9320191019https://doi.org/10.1259/bjr.20191019
        • Valente S.A.
        • Levine G.M.
        • Silverstein M.J.
        • et al.
        Accuracy of predicting axillary lymph node positivity by physical examination, mammography, ultrasonography, and magnetic resonance imaging.
        Ann Surg Oncol. 2012; 19: 1825-1830https://doi.org/10.1245/s10434-011-2200-7
        • Peppe A.
        • Wilson R.
        • Pope R.
        • et al.
        The use of ultrasound in the clinical re-staging of the axilla after neoadjuvant chemotherapy (NACT).
        Breast. 2017; 35: 104-108https://doi.org/10.1016/j.breast.2017.05.015
        • Shetty M.K.
        • Carpenter W.S.
        Sonographic evaluation of isolated abnormal axillary lymph nodes identified on mammograms.
        J Ultrasound Med. 2004; 23: 63-71https://doi.org/10.7863/jum.2004.23.1.63
        • van Nijnatten T.J.A.
        • Ploumen E.H.
        • Schipper R.J.
        • et al.
        Routine use of standard breast MRI compared to axillary ultrasound for differentiating between no, limited and advanced axillary nodal disease in newly diagnosed breast cancer patients.
        Eur J Radiol. 2016; 85: 2288-2294https://doi.org/10.1016/j.ejrad.2016.10.030
        • Zhang L.
        • Huang Y.
        • Yang C.
        • et al.
        Application of a carbon nanoparticle suspension for sentinel lymph node mapping in patients with early breast cancer: a retrospective cohort study.
        World J Surg Oncol. 2018; 16: 112https://doi.org/10.1186/s12957-018-1414-6
        • for the S.G.
        • Agha R
        • Abdall-Razak A
        • et al.
        STROCSS 2019 guideline: strengthening the reporting of cohort studies in surgery.
        Int J Surg. 2019; 72: 156-165https://doi.org/10.1016/j.ijsu.2019.11.002
        • Gradishar W.J.
        • Anderson B.O.
        • Blair S.L.
        • et al.
        Breast cancer version 3.2014.
        J Nat Comprehens Cancer Network : JNCCN. 2014; 12: 542-590https://doi.org/10.6004/jnccn.2014.0058
        • Mamounas E.P.
        • Brown A.
        • Anderson S.
        • 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: 2694-2702https://doi.org/10.1200/JCO.2005.05.188
        • Hieken T.J.
        • Boughey J.C.
        • Jones K.N.
        • et al.
        Imaging response and residual metastatic axillary lymph node disease after neoadjuvant chemotherapy for primary breast cancer.
        Ann Surg Oncol. 2013; 20: 3199-3204https://doi.org/10.1245/s10434-013-3118-z
        • You S.
        • Kang D.K.
        • Jung Y.S.
        • et al.
        Evaluation of lymph node status after neoadjuvant chemotherapy in breast cancer patients: comparison of diagnostic performance of ultrasound, MRI and 18F-FDG PET/CT.
        Br J Radiol. 2015; 8820150143https://doi.org/10.1259/bjr.20150143
        • Ha S.M.
        • Cha J.H.
        • Kim H.H.
        • et al.
        Diagnostic performance of breast ultrasonography and MRI in the prediction of lymph node status after neoadjuvant chemotherapy for breast cancer.
        Acta Radiologica (Stockholm, Sweden : 1987). 2017; 58: 1198-1205https://doi.org/10.1177/0284185117690421
        • Cheng M.
        • Zhuang X.
        • Zhang L.
        • et al.
        A nomogram to predict non-sentinel lymph node metastasis in patients with initial cN+ breast cancer that downstages to cN0 after neoadjuvant chemotherapy.
        J Surg Oncol. 2020; 122: 373-381https://doi.org/10.1002/jso.25989
        • Goyal A.
        • Newcombe R.G.
        • Chhabra A.
        • et al.
        Factors affecting failed localisation and false-negative rates of sentinel node biopsy in breast cancer–results of the ALMANAC validation phase.
        Breast Cancer Res Treat. 2006; 99: 203-208https://doi.org/10.1007/s10549-006-9192-1
        • Tafra L.
        • Lannin D.R.
        • Swanson M.S.
        • et al.
        Multicenter trial of sentinel node biopsy for breast cancer using both technetium sulfur colloid and isosulfan blue dye.
        Ann Surg. 2001; 233: 51-59https://doi.org/10.1097/00000658-200101000-00009
        • Kim G.R.
        • Choi J.S.
        • Han B.-K.
        • et al.
        Preoperative axillary us in early-stage breast cancer: potential to prevent unnecessary axillary lymph node dissection.
        Radiology. 2018; 288: 55-63https://doi.org/10.1148/radiol.2018171987
        • Barron A.U.
        • Hoskin T.L.
        • Boughey J.C.
        Predicting non-sentinel lymph node metastases in patients with a positive sentinel lymph node after neoadjuvant chemotherapy.
        Ann Surg Oncol. 2018; 25: 2867-2874https://doi.org/10.1245/s10434-018-6578-3
        • Evrensel T.
        • Johnson R.
        • Ahrendt G.
        • et al.
        The predicted probability of having positive non-sentinel lymph nodes in patients who received neoadjuvant chemotherapy for large operable breast cancer.
        Int J Clin Pract. 2008; 62: 1379-1382https://doi.org/10.1111/j.1742-1241.2006.01265.x
        • Zhang K.
        • Zhu Q.
        • Sheng D.
        • et al.
        A new model incorporating axillary ultrasound after neoadjuvant chemotherapy to predict non-sentinel lymph node metastasis in invasive breast cancer.
        Cancer Manage Res. 2020; 12: 965-972https://doi.org/10.2147/CMAR.S239921
        • Yu Y.
        • He Z.
        • Ouyang J.
        • et al.
        Magnetic resonance imaging radiomics predicts preoperative axillary lymph node metastasis to support surgical decisions and is associated with tumor microenvironment in invasive breast cancer: A machine learning, multicenter study.
        EBioMedicine. 2021; 69103460https://doi.org/10.1016/j.ebiom.2021.103460
        • Yang Y
        • He Y
        • Fan Z
        • et al.
        A new model to predict risk of nonsentinel lymph node status in Chinese sentinel lymph node-positive patients after neoadjuvant chemotherapy.
        Breast J. 2018; 24: 883-888https://doi.org/10.1111/tbj.13065
        • Zhang K
        • Zhu Q
        • Sheng D
        • et al.
        A new model incorporating axillary ultrasound after neoadjuvant chemotherapy to predict non-sentinel lymph node metastasis in invasive breast cancer.
        Cancer Management Res. 2020; 12: 965-972https://doi.org/10.2147/CMAR.S239921
        • Zhu J
        • Jiao D
        • Yan M
        • et al.
        Establishment and verification of a predictive model for node pathological complete response after neoadjuvant chemotherapy for initial node positive early breast cancer.
        Front Oncol. 2021; 11: 1-9https://doi.org/10.3389/fonc.2021.675070