Pre-operative Ultrasonographic Evaluation of Axillary Lymph Nodes in Breast Cancer Patients: For Which Group Still of Additional Value and in Which Group Cause for Special Attention?

doi:10.1016/j.ultrasmedbio.2015.06.013

Ultrasound in Medicine & Biology

Volume 41, Issue 11, November 2015, Pages 2842-2848

https://doi.org/10.1016/j.ultrasmedbio.2015.06.013 Get rights and content

Abstract

A non-invasive and widely available method for pre-operative evaluation of the axilla is axillary ultrasonography (US). The purpose of this study was to evaluate the diagnostic accuracy of axillary US and fine-needle aspiration cytology in a large cohort of breast cancer patients. The sensitivity and specificity of US and fine-needle aspiration cytology in our cohort of 1124 patients were 42.2% and 97.1%, respectively. As the number of axillary nodes increased, sensitivity increased. The percentage of false-negative US results was 18.9%; patients in this subgroup were significantly younger, had larger tumors, more often had lymph vascular invasion and were more likely to have estrogen receptor-positive tumors. Ultrasonography in combination with fine-needle aspiration cytology is useful in the pre-operative workup of breast cancer patients, especially patients with three or more nodal metastases. Special attention should be paid to younger women with larger tumors in whom a larger percentage of false-negative results are obtained.

Introduction

Over the years there has been growing interest in the development of clinical prediction tools to estimate the risk of patients with breast cancer having axillary nodal metastases, thereby making it possible to plan specific therapies. Sentinel lymph node biopsy (SLNB) has become the standard method of axillary lymph node staging in patients with invasive breast cancer. It has replaced axillary lymph node dissection (ALND), as it is associated with significantly lower morbidity (Purushotham et al. 2005). However, SLNB is still an invasive method and has a 4%–14% rate of complications such as lymphedema, seroma, paresthesia, chronic pain and immobility (Temple et al. 2002). When node metastases are found with SLNB, ALND is still warranted, which means that the patient has to undergo a second operation. Not only is this an inconvenience for the patient, but it also results in more operating time, space and costs (Boughey et al. 2010).

A non-invasive and widely available screening method is axillary ultrasonography (US). Pre-operative axillary US, with or without fine-needle aspiration cytology (FNAC) of lymph nodes suspicious for metastases, is now routinely performed in many breast cancer centers (Glynn et al. 2010). The utility of axillary US in detecting nodal metastases has been studied extensively. The results vary widely, especially in patients with early-stage breast cancer (Alvarez et al., 2006, Garcia Fernandez et al., 2011, Mainiero et al., 2010). The sensitivity and specificity of axillary US range between 40% and 92%, and between 56% and 100%, respectively. Specificity increases to 100% with the use of FNAC. However, as with all US procedures, the sensitivity and specificity of axillary US depend strongly on the experience of the ultrasonographer and the reference standard for malignancy used. The majority of previous studies on axillary US and FNAC have studied small patient groups (<500 patients) and have used different morphologic criteria for detecting nodal metastases: palpable versus non-palpable nodes, inclusion or exclusion of micrometastases and differences in the prevalence of axillary nodal burden (Alvarez et al., 2006, Bonnema et al., 1997, Cho et al., 2009, De Freitas et al., 1991, Jung et al., 2010, Motomura et al., 2001, Rajesh et al., 2002, Vaidya et al., 1996, Verbanck et al., 1997, Yang et al., 1996).

The aim of this study was to evaluate the utility and diagnostic accuracy of axillary US and US with FNAC in detecting axillary lymph node metastases in a large cohort of breast cancer patients.

Section snippets

Patients

This retrospective cohort study was conducted in the Hospital Group Twente, a large teaching hospital located in Almelo and Hengelo, The Netherlands. Approval from the institutional review board was not required because this was a non-interventional retrospective study using known data. From January 2007 until July 2011, 1124 consecutive primary breast cancer patients were selected. These patients were both screen detected and/or symptomatic. All patients underwent pre-operative axillary US and

Patient and tumor characteristics

During the observational period from January 2007 until July 2011, 1178 patients were treated for primary invasive breast cancer in the Hospital Group Twente, The Netherlands. Of these patients, 20 had palpable axillary lymph nodes and 34 patients, did not undergo the routine workup for other reasons, leaving 1124 patients for further analysis. All patients had solitary tumors. The median age of the patients was 61 y (range: 24–93 y). The mean primary breast cancer tumor size was 20.46 mm

Discussion

In the present study, we assessed the accuracy and clinical utility of routine pre-operative axillary US in combination with FNAC in patients with breast cancer in The Netherlands. The prevalence of nodal metastases (macrometastases) in our study was 28.4%. Our study suggests that specificity and PPV in detecting axillary metastases were higher for patients who underwent axillary US in combination with FNAC, especially those with gross nodal disease, than for patients who underwent US alone.

Conclusions

Ultrasonography in combination with FNAC is useful in the pre-operative workup of breast cancer patients. Patients with early-stage breast cancer are unlikely to have heavy axillary disease burden, and in this subgroup the value of ALND has recently been up for discussion. Within the group of patients with three or more nodal metastases, however, the accuracy of US and FNAC is much higher and will be of additional value. Special attention should be paid to younger woman with larger tumors, in

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Pre-operative Conventional Ultrasound and Sonoelastography Evaluation for Predicting Axillary Lymph Node Metastasis in Patients with Malignant Breast Lesions
2018, Ultrasound in Medicine and Biology
Citation Excerpt :
Axillary lymph node status in breast cancer is one of the most important prognostic indicators of clinical outcome and influences treatment decisions (Fisher et al. 2002). Although axillary conventional ultrasound (US) and contrast-enhanced US (CEUS) have become important approaches in screening axillary lymph nodes for breast cancer, both techniques not only are affected strongly by the operator's experience, but also fail to detect small or deeply located lymph nodes (Moorman et al. 2015). As a conventional operation to determine whether axillary lymph node dissection should be performed in surgery for breast cancer, sentinel lymph node biopsy is invasive and associated with complications such as lymphedema, paresthesia, chronic pain and immobility, with an incidence rate of 4%–14% (Temple et al. 2002).
The objective of our study was to evaluate the association between the sonoelastography features of breast tumor and axillary lymph node metastasis (ALNM) in patients with breast cancer. In a cohort of 106 women with breast cancer, the conventional ultrasound features and elasticity parameters by elasticity imaging and Virtual Touch Tissue Imaging & Quantification (VTIQ) were retrospectively analyzed. Ultrasound and elastography findings were compared with pathologic axillary lymph node status. Receiver operating characteristic curve analysis was used to evaluate diagnostic performance. Pathologically, the overall incidence of ALNM was 39.6% (42/106) in the final analysis. ALNM was significantly more frequent in tumors with elasticity imaging scores >4.5, maximal shear wave velocity values (S_max) >6.42 m/s and mean shear wave velocity values (S_mean) >5.66 m/s, respectively. The sensitivity, specificity and accuracy were 78.6%, 54.7% and 64.2% for elasticity imaging score; 85.7%, 54.7% and 67.0% for S_max; and 59.5%, 79.7% and 71.7% for S_mean, respectively Elastography features, including elasticity imaging score and VTIQ, can be used to supplement conventional ultrasound to predict ALNM in patients with breast cancers.
Value of ultrasound-guided fine needle aspiration in diagnosing axillary lymph node recurrence after breast cancer surgery
2018, American Journal of Surgery
Citation Excerpt :
Fortunately, early detection of locoregional recurrence or contralateral breast cancer has been associated with improved survival.8–10 Whereas the diagnostic accuracy of US-FNA of ALNs has been reported to be affected by clinical-pathologic factors in patients with newly diagnosed breast cancer, to our knowledge, there are currently no studies evaluating its diagnostic accuracy in patients with a history of breast cancer surgery.11–14 Therefore, the purpose of this study was to assess the diagnostic performance of US-FNA in detecting ALN recurrence in patients with a history of breast cancer.
This article aims to assess the diagnostic performance of ultrasound-guided fine needle aspiration (US-FNA) in diagnosing axillary lymph node (ALN) recurrence in patients with a history of breast cancer.
From January 2005 to June 2015, 231 US-FNA examinations performed for suspicious axillary lesions in 218 patients with a history of breast cancer were included. Diagnostic performance of US-FNA for ALN recurrence were evaluated.
Of the 231 US-FNA examinations, 172 (74.5%) obtained negative and 59 (25.5%) obtained positive cytological results. All US-FNA-negative axillary lesions were considered imaging-cytology concordant and underwent follow-up, with one false-negative result (false negative rate, 1.6% [1/60]). The overall sensitivity, specificity, PPV and NPV of US-FNA for diagnosing ALN recurrence/metastasis per examination were 98.3% (59/60), 100% (171/171), 100% (59/59) and 99.4% (171/172). When excluding nine patients with newly developed contralateral breast cancer, the sensitivity, specificity, PPV and NPV of US-FNA for diagnosing ALN recurrence was 98.1% (51/52),100% (170/170),100% (51/51) and 99.4% (170/171).
US-FNA is a reliable method for diagnosing axillary recurrence in patients with a history of breast cancer.
ACR Appropriateness Criteria<sup>®</sup> Monitoring Response to Neoadjuvant Systemic Therapy for Breast Cancer
2017, Journal of the American College of Radiology
Citation Excerpt :
By identifying pathologic-appearing nodes, US-guided FNA or core biopsy can confirm metastatic disease, thereby obviating the need for pretreatment sentinel node biopsy because the completion of axillary node dissection is typically performed after completion of therapy [2,106]. However, as axillary US has false-negative rates of up to 20%, surgical staging of the axilla before neoadjuvant therapy is important to determine the most appropriate management [107-109]. The axilla is often visualized, permitting identification of pathologic lymphadenopathy.
Patients with locally advanced invasive breast cancers are often treated with neoadjuvant chemotherapy prior to definitive surgical intervention. The primary aims of this approach are to: 1) reduce tumor burden thereby permitting breast conservation rather than mastectomy; 2) promptly treat possible metastatic disease, whether or not it is detectable on preoperative staging; and 3) potentially tailor future chemotherapeutic decisions by monitoring in-vivo tumor response. Accurate radiological assessment permits optimal management and planning in this population. However, assessment of tumor size and response to treatment can vary depending on the modality used, the measurement technique (such as single longest diameter, 3-D measurements, or calculated tumor volume), and varied response of different tumor subtypes to neoadjuvant chemotherapy (such as concentric shrinkage or tumor fragmentation). As discussed in further detail, digital mammography, digital breast tomosynthesis, US and MRI represent the key modalities with potential to help guide patient management.
The American College of Radiology Appropriateness Criteria are evidence-based guidelines for specific clinical conditions that are reviewed annually by a multidisciplinary expert panel. The guideline development and revision include an extensive analysis of current medical literature from peer reviewed journals and the application of well-established methodologies (RAND/UCLA Appropriateness Method and Grading of Recommendations Assessment, Development, and Evaluation or GRADE) to rate the appropriateness of imaging and treatment procedures for specific clinical scenarios. In those instances where evidence is lacking or equivocal, expert opinion may supplement the available evidence to recommend imaging or treatment.
Axillary Lymph Node Sonographic Features and Breast Tumor Characteristics as Predictors of Malignancy: A Nomogram to Predict Risk
2017, Ultrasound in Medicine and Biology
Citation Excerpt :
The FNA findings from our study (36.4% sensitivity and 97.6% specificity) are consistent with those of Alvarez et al. (2006), who reported a lymph node biopsy sensitivity between 30.6% (22.5%–39.6%) and 62.9% (49.7%–74.8%) and a specificity of 100% (94.8%–100%). Our data are also concordant with a recent report from Moorman et al. (2015), who found 42.2% sensitivity and 97.1% specificity for lymph node biopsies. In contrast to Koelliker et al. (2008), our study suggested that performing FNA of lymph nodes that are classified as normal on ultrasonography was not beneficial because none of the lymph nodes classified as normal were positive on FNA.
The purpose of this study was to build a mathematical model to predict the probability of axillary lymph node metastasis based on the ultrasonographic features of axillary lymph nodes and the tumor characteristics. We included 74 patients (75 axillae) with invasive breast cancer who underwent axillary ultrasonography ipsilateral to the tumor and fine-needle aspiration of one selected lymph node. Lymph node pathology results from sentinel lymph node biopsy or surgical dissection were correlated with lymph node ultrasonographic data and with the cytologic findings of fine-needle aspiration. Our mathematical model of prediction risk of lymph node metastasis included only pre-surgical data from logistic regression analysis: lymph node cortical thickness (p = 0.005), pre-surgical tumor size (p = 0.030), menopausal status (p = 0.017), histologic type (p = 0.034) and tumor location (p = 0.011). The area under the receiver operating characteristic curve of the model was 0.848, reflecting an excellent discrimination of the model. This nomogram may assist in the choice of the optimal axillary approach.
Pre-Operative Evaluation of Axillary Lymph Node Status in Patients with Suspected Breast Cancer Using Shear Wave Elastography
2017, Ultrasound in Medicine and Biology
Citation Excerpt :
In patients with newly diagnosed breast cancer, pre-operative evaluation of axillary lymph node status is critical as an integral component of breast cancer management, including staging, treatment plan and prognosis (Fisher et al. 1983; Humphrey et al. 2014). Ultrasound has been performed for non-invasive pre-operative evaluation of the axillary nodal basin because it is widely available and easily incorporated into the standard workup for breast cancer patients (Moorman et al. 2015). Sonographic criteria based on size (>5 mm) or morphologic characteristics (round, hypo-echoic, with loss of central hilum, eccentric cortical hypertrophy) have exhibited varied diagnostic performance for metastatic lymph nodes (Alvarez et al. 2006).
The aim of this study was to evaluate shear wave elastography (SWE) for pre-operative evaluation of axillary lymph node (LN) status in patients with suspected breast cancer. A total of 130 axillary LNs in 130 patients who underwent SWE before fine-needle aspiration, core biopsy or surgery were analyzed. On gray-scale images, long and short axes, shape (elliptical or round), border (sharp or unsharp) and cortical thickening (concentric, eccentric or no fatty hilum) of LNs were assessed. On SWE, mean, maximum, minimum, standard deviation and the lesion-to-fat ratio (E_ratio) values of elasticity were collected. Gray-scale and SWE features were compared statistically between metastatic and benign LNs using the χ²-test and independent t-test. Diagnostic performance of each feature was evaluated using the area under the receiver operating characteristic curve (AUC). Logistic regression analysis was used to determine gray-scale or SWE features independently associated with metastatic LNs. Of the 130 LNs, 65 (50%) were metastatic and 65 (50%) were benign after surgery. Metastatic LNs were significantly larger (p = 0.018); had higher elasticity indexes at SWE (p < 0.0001); and had higher proportions of round shape (p = 0.033), unsharp border (p = 0.048) and eccentric cortical thickening or no fatty hilum (p = 0.005) compared with benign LNs. On multivariate analysis, E_ratio was independently associated with metastatic LNs (odds ratio = 3.312, p = 0.008). E_ratio had the highest AUC among gray-scale (0.582–0.719) and SWE (0.900–0.950) variables. SWE had good diagnostic performance in metastatic axillary LNs, and E_ratio was independently associated with metastatic LNs.
Axillary lymph node status in breast cancer patients: Preoperative assessment and management's evolution
2017, Imagerie de la Femme
Le statut ganglionnaire axillaire reste un des facteurs pronostiques les plus importants dans la prise en charge du cancer du sein et sa connaissance avant la chirurgie est nécessaire pour le choix thérapeutique. Les différentes modalités d’imagerie ont été évaluées pour la détection préopératoire des métastases ganglionnaires axillaires de cancers du sein. Bien qu’aucune des modalités ne soit suffisamment fiable, l’examen de choix reste l’échographie axillaire, avec des critères simples, associée à la cytoponction ou à la microbiopsie des ganglions échographiquement suspects. Cependant, la prise en charge des patientes N+ évolue et cet examen est remis en question par plusieurs études, ce qui a poussé à créer des scores de risque d’envahissement ganglionnaire.
Axillary lymph node status is still one of most important prognostic factors in breast cancer and it is necessary to evaluate it preoperatively for therapeutic choice. All imaging modalities were evaluated to detect preoperatively axillary lymph node metastases. Although none is enough reliable, axillary ultrasound, with simple criteria, associated with fine-needle-aspiration-cytology or core-biopsy of suspect lymph nodes, still remains the best modality. However, management of N+ patients evolves and axillary ultrasound is questioned by several studies, which urged to develop nomograms and predictive scores of metastatic axillary lymph node status.

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: Conflict of interest disclosure: None of the authors declare any conflict of interest.

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Original ContributionPre-operative Ultrasonographic Evaluation of Axillary Lymph Nodes in Breast Cancer Patients: For Which Group Still of Additional Value and in Which Group Cause for Special Attention?

Abstract

Introduction

Section snippets

Patients

Patient and tumor characteristics

Discussion

Conclusions

Ultrasound Med Biol

Eur J Cancer

Ultrasound Med Biol

Eur J Radiol

Am J Surg

Clin Radiol

Eur J Cancer

Breast

Eur J Surg Oncol

Breast

Eur J Surg Oncol

Axillary lymph node echo-guided fine-needle aspiration cytology enables breast cancer patients to avoid a sentinel lymph node biopsy. Preliminary experience and a review of the literature

Surg Today

Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: A systematic review

AJR Am J Roentgenol

Ultrasound-guided aspiration biopsy for detection of nonpalpable axillary node metastases in breast cancer patients: New diagnostic method

World J Surg

Cost modeling of preoperative axillary ultrasound and fine-needle aspiration to guide surgery for invasive breast cancer

Ann Surg Oncol

Preoperative sonographic classification of axillary lymph nodes in patients with breast cancer: Node-to-node correlation with surgical histology and sentinel node biopsy results

AJR Am J Roentgenol

Preoperative axillary ultrasound and fine-needle aspiration biopsy in the diagnosis of axillary metastases in patients with breast cancer: predictors of accuracy and future implications

Ann Surg Oncol

Accuracy of ultrasound and clinical examination in the diagnosis of axillary lymph node metastases in breast cancer

Eur J Surg Oncol

Original Contribution
Pre-operative Ultrasonographic Evaluation of Axillary Lymph Nodes in Breast Cancer Patients: For Which Group Still of Additional Value and in Which Group Cause for Special Attention?