Abstract
Objective
This systematic review examined the diagnostic performance of magnetic resonance imaging (MRI) for assessing axillary lymph node status (ALNS) after neoadjuvant chemotherapy (NAC) in breast cancer patients.
Methods
We searched PubMed, Embase, Cochrane Library, and Web of Science to identify relevant studies and used the QUADAS-2 tool to assess methodological quality of eligible studies. We used STATA version 12.0 to perform data pooling, heterogeneity testing, subgroup analysis, and sensitivity analysis.
Results
For the 21 enrolled studies, including 2875 patients, the pooled sensitivity, specificity, positive likelihood ratio, negative likelihood ratio, and diagnostic odds ratio were respectively 0.63 (95% CI: 0.53–0.72), 0.75 (95% CI: 0.68–0.81), 2.52 (95% CI: 1.98–3.19), 0.50 (95% CI: 0.39–0.63), and 5.08 (95% CI: 3.38–7.63). The AUC was 0.76 (95% CI: 0.72–0.79). I2 values of sensitivity (I2 = 94.41%) and specificity (I2 = 88.97%) were both > 50%. For the initial positive ALN patients, the pooled sensitivity and specificity were 0.64 (95% CI: 0.53–0.75) and 0.74 (95% CI: 0.64–0.82), respectively. Sensitivity analyses by focusing on studies with MRI performed post-NAC, studies using DCE-MRI, or studies with low risk of bias showed similar results to the primary analyses.
Conclusion
MRI may have suboptimal diagnostic value in assessing ALNS after NAC for breast cancer patients. Due to the inconsistency of NAC regimens, the variability of axillary surgery, and the lack of time interval between MRI and surgery, further studies are needed to confirm our findings.
Clinical relevance statement
Our study provided the diagnostic value of MRI in assessing axillary lymph node status after neoadjuvant chemotherapy for breast cancer patients.
Key Points
• MRI may have suboptimal diagnostic value in assessing axillary lymph node status after NAC for general breast cancer patients.
• The initial axillary lymph node status has little impact on the diagnostic efficacy of MRI.
• The substantial heterogeneity among studies highlights the need for further studies to provide more high-quality evidence in this field.
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Abbreviations
- ALNS:
-
Axillary lymph node status
- DOR:
-
Diagnostic odds ratio
- MRI:
-
Magnetic resonance imaging
- NAC:
-
Neoadjuvant chemotherapy
- NLR:
-
Negative likelihood ratio
- PLR:
-
Positive likelihood ratio
- PRISMA-DTA:
-
Preferred Reporting Items for Systematic Reviews and Meta-Analyses of Diagnostic Test Accuracy Studies
- QUADAS-2:
-
Quality Assessment of Diagnostic Accuracy Studies-2
References
Korde LA, Somerfield MR, Carey LA et al (2021) Neoadjuvant chemotherapy, endocrine therapy, and targeted therapy for breast cancer: ASCO guideline. J Clin Oncol 39:1485–1505
Rouzier R, Extra JM, Klijanienko J et al (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 20:1304–1310
Mamounas EP, Anderson SJ, Dignam JJ et al (2012) Predictors of locoregional recurrence after neoadjuvant chemotherapy: results from combined analysis of National Surgical Adjuvant Breast and Bowel Project B-18 and B-27. J Clin Oncol 30:3960–3966
Ivens D, Hoe AL, Podd TJ, Hamilton CR, Taylor I, Royle GT (1992) Assessment of morbidity from complete axillary dissection. Br J Cancer 66:136–138
Koelliker SL, Chung MA, Mainiero MB, Steinhoff MM, Cady B (2008) Axillary lymph nodes: US-guided fine-needle aspiration for initial staging of breast cancer–correlation with primary tumor size. Radiology 246:81–89
Veronesi U, Paganelli G, Galimberti V et al (1997) Sentinel-node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph-nodes. Lancet 349:1864–1867
Dialani V, Chadashvili T, Slanetz PJ (2015) Role of imaging in neoadjuvant therapy for breast cancer. Ann Surg Oncol 22:1416–1424
Tateishi U, Miyake M, Nagaoka T et al (2012) Neoadjuvant chemotherapy in breast cancer: prediction of pathologic response with PET/CT and dynamic contrast-enhanced MR imaging–prospective assessment. Radiology 263:53–63
Li Z, Gao Y, Gong H et al (2023) Different imaging modalities for the diagnosis of axillary lymph node metastases in breast cancer: a systematic review and network meta-analysis of diagnostic test accuracy. J Magn Reson Imaging 57:1392–1403
Samiei S, de Mooij CM, Lobbes MBI, Keymeulen K, van Nijnatten TJA, Smidt ML (2021) Diagnostic performance of noninvasive imaging for assessment of axillary response after neoadjuvant systemic therapy in clinically node-positive breast cancer: a systematic review and meta-analysis. Ann Surg 273:694–700
McInnes MDF, Moher D, Thombs BD et al (2018) Preferred Reporting Items for a Systematic Review and Meta-analysis of Diagnostic Test Accuracy Studies: the PRISMA-DTA statement. JAMA 319:388–396
Whiting PF, Rutjes AW, Westwood ME et al (2011) QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 155:529–536
Abel MK, Greenwood H, Kelil T et al (2021) Accuracy of breast MRI in evaluating nodal status after neoadjuvant therapy in invasive lobular carcinoma. NPJ Breast Cancer 7:25
Beek MA, Tetteroo E, Luiten EJ et al (2016) Clinical impact of breast MRI with regard to axillary reverse mapping in clinically node positive breast cancer patients following neo-adjuvant chemotherapy. Eur J Surg Oncol 42:672–678
Cortina CS, Gottschalk N, Kulkarni SA, Karst I (2021) Is breast magnetic resonance imaging an accurate predictor of nodal status after neoadjuvant chemotherapy? J Surg Res 257:412–418
Eun NL, Son EJ, Gweon HM, Kim JA, Youk JH (2020) Prediction of axillary response by monitoring with ultrasound and MRI during and after neoadjuvant chemotherapy in breast cancer patients. Eur Radiol 30:1460–1469
Graña-López L, Pérez-Ramos T, Maciñeira FA, Villares Á, Vázquez-Caruncho M (2022) Predicting axillary response to neoadjuvant chemotherapy: the role of diffusion weighted imaging. Br J Radiol 95:20210511
Ha SM, Cha JH, Kim HH, Shin HJ, Chae EY, Choi WJ (2017) Diagnostic performance of breast ultrasonography and MRI in the prediction of lymph node status after neoadjuvant chemotherapy for breast cancer. Acta Radiol 58:1198–1205
Hieken TJ, Boughey JC, Jones KN, Shah SS, Glazebrook KN (2013) Imaging response and residual metastatic axillary lymph node disease after neoadjuvant chemotherapy for primary breast cancer. Ann Surg Oncol 20:3199–3204
Hsiang DJ, Yatnamoto M, McHta RS et al (2007) Predicting nodal status using dynamic contrast-enhanced magnetic resonance imaging in patients with locally advanced breast cancer undergoing neoadjuvant chemotherapy with and without sequential trastuzumab. Arch Surg 142:855–860
Hyun SJ, Kim EK, Moon HJ, Yoon JH, Kim MJ (2016) Preoperative axillary lymph node evaluation in breast cancer patients by breast magnetic resonance imaging (MRI): can breast MRI exclude advanced nodal disease? Eur Radiol 26:3865–3873
İrİaǧaç Y, Karaboyun K, Çavdar E et al (2022) The diagnostic contribution of magnetic resonance imaging in the detection of axillary metastasis after neoadjuvant chemotherapy. Neoplasma 69:741–746
Javid S, Segara D, Lotfi P, Raza S, Golshan M (2010) Can breast MRI predict axillary lymph node metastasis in women undergoing neoadjuvant chemotherapy. Ann Surg Oncol 17:1841–1846
Kim TH, Kang DK, Kim JY, Han S, Jung Y (2015) Histologic grade and decrease in tumor dimensions affect axillary lymph node status after neoadjuvant chemotherapy in breast cancer patients. J Breast Cancer 18:394–399
Mattingly AE, Mooney B, Lin HY et al (2017) Magnetic resonance imaging for axillary breast cancer metastasis in the neoadjuvant setting: a prospective study. Clin Breast Cancer 17:180–187
Moo TA, Jochelson MS, Zabor EC et al (2019) Is clinical exam of the axilla sufficient to select node-positive patients who downstage after NAC for SLNB? A comparison of the accuracy of clinical exam versus MRI. Ann Surg Oncol 26:4238–4243
Murphy LC, Quinn EM, Razzaq Z et al (2020) Assessing the accuracy of conventional gadolinium-enhanced breast MRI in measuring the nodal response to neoadjuvant chemotherapy (NAC) in breast cancer. Breast J 26:2151–2156
Sobhi A, TalaatHamed S, Hussein ES, Lasheen S, Hussein M, Ebrahim Y (2022) Predicting pathological response of locally advanced breast cancer to neoadjuvant chemotherapy: comparing the performance of whole body 18F-FDG PETCT versus DCE-MRI of the breast. Egypt J Radiol Nucl Med 53:79
Steiman J, Soran A, McAuliffe P et al (2016) Predictive value of axillary nodal imaging by magnetic resonance imaging based on breast cancer subtype after neoadjuvant chemotherapy. J Surg Res 204:237–241
Turan U, Aygun M, Duman BB et al (2021) Efficacy of US, MRI, and F-18 FDG-PET/CT for detecting axillary lymph node metastasis after neoadjuvant chemotherapy in breast cancer patients. Diagnostics 11:2361
Weber JJ, Jochelson MS, Eaton A et al (2017) MRI and prediction of pathologic complete response in the breast and axilla after neoadjuvant chemotherapy for breast cancer. J Am Coll Surg 225:740–746
Woo J, Ryu JM, Jung SM et al (2021) Breast radiologic complete response is associated with favorable survival outcomes after neoadjuvant chemotherapy in breast cancer. Eur J Surg Oncol 47:232–239
You S, Kang DK, Jung YS, An YS, Jeon GS, Kim TH (2015) Evaluation of lymph node status after neoadjuvant chemotherapy in breast cancer patients: comparison of diagnostic performance of ultrasound, MRI and F-18-FDG PET/CT. Br J Radiol 88:20150143
Liang X, Yu J, Wen B, Xie J, Cai Q, Yang Q (2017) MRI and FDG-PET/CT based assessment of axillary lymph node metastasis in early breast cancer: a meta-analysis. Clin Radiol 72:295–301
Zhou P, Wei Y, Chen G, Guo L, Yan D, Wang Y (2018) Axillary lymph node metastasis detection by magnetic resonance imaging in patients with breast cancer: a meta-analysis. Thorac Cancer 9:989–996
Tudorica A, Oh KY, Chui SY et al (2016) Early prediction and evaluation of breast cancer response to neoadjuvant chemotherapy using quantitative DCE-MRI. Transl Oncol 9:8–17
O’Connor JP, Jackson A, Parker GJ, Roberts C, Jayson GC (2012) Dynamic contrast-enhanced MRI in clinical trials of antivascular therapies. Nat Rev Clin Oncol 9:167–177
Leach MO, Morgan B, Tofts PS et al (2012) Imaging vascular function for early stage clinical trials using dynamic contrast-enhanced magnetic resonance imaging. Eur Radiol 22:1451–1464
Padhani AR, Miles KA (2010) Multiparametric imaging of tumor response to therapy. Radiology 256:348–364
Wasser K, Sinn HP, Fink C et al (2003) Accuracy of tumor size measurement in breast cancer using MRI is influenced by histological regression induced by neoadjuvant chemotherapy. Eur Radiol 13:1213–1223
Schipper RJ, Moossdorff M, Beets-Tan RGH, Smidt ML, Lobbes MBI (2015) Noninvasive nodal restaging in clinically node positive breast cancer patients after neoadjuvant systemic therapy: a systematic review. Eur J Radiol 84:41–47
Hosny A, Parmar C, Quackenbush J, Schwartz LH, Aerts H (2018) Artificial intelligence in radiology. Nat Rev Cancer 18:500–510
Gan L, Ma M, Liu Y et al (2021) A clinical-radiomics model for predicting axillary pathologic complete response in breast cancer with axillary lymph node metastases. Front Oncol 11:786346
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Li, Z., Ma, Q., Gao, Y. et al. Diagnostic performance of MRI for assessing axillary lymph node status after neoadjuvant chemotherapy in breast cancer: a systematic review and meta-analysis. Eur Radiol 34, 930–942 (2024). https://doi.org/10.1007/s00330-023-10155-8
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DOI: https://doi.org/10.1007/s00330-023-10155-8