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ORIGINAL ARTICLE Table of Contents  
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Diagnostic accuracy of ultrasonography in axillary staging in breast cancer patients

1 Department of General Surgery, James Cook University Hospital, Middlesbrough, UK
2 Foundation Doctor, Misr University for Science and Technology, Giza, Egypt

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Date of Submission27-Sep-2022
Date of Decision25-Oct-2022
Date of Acceptance30-Nov-2022
Date of Web Publication14-Feb-2023


Background: Breast cancer is the most common malignancy affecting women all over the world and represents 7% of all cancer-related deaths in the UK. One of the most crucial elements in assessing a patient's prognosis and chance of survival with breast cancer is the condition of their axillary lymph nodes. Ultrasonography (US) is now used as a routine preoperative diagnostic tool for pretherapeutic axillary evaluation. The aim of the current study is to investigate the diagnostic accuracy of US in axillary staging in breast cancer patients. Methods: We carried out this retrospective study for all invasive breast cancer patients who had surgery in addition to preoperative axillary staging using US during the period from January 2020 to February 2021. The final histology results were compared with the preoperative US findings to ascertain the sensitivity, specificity, positive predictive value, and negative predictive value of AUS in axillary staging. Results: One hundred and twenty-eight patients were included in our study. The average age of diagnosis was 63.9 ± 12.3 years of age. We calculated sensitivity rate of 59.6%, specificity rate of 95.1%, positive predictive value of 87.5%, and negative predictive value of 80.2% with overall diagnostic accuracy of 82.2%. Conclusion: Despite the important role of preoperative US in axillary staging in breast cancer patients; it failed to detect metastatic diseases in 14.8% of our patients. These findings necessitate the routine histological evaluation of the axilla for more accurate staging of the disease.

Keywords: Axilla, breast cancer, diagnostic accuracy, histology, ultrasonography

How to cite this URL:
Nassif Rezkallah EM, Elsaify A, Min Tin SM, Elsaify W. Diagnostic accuracy of ultrasonography in axillary staging in breast cancer patients. J Med Ultrasound [Epub ahead of print] [cited 2023 Mar 22]. Available from: http://www.jmuonline.org/preprintarticle.asp?id=369637

  Introduction Top

Breast cancer is the most frequent cancer among women worldwide.[1] Breast cancer is responsible for 15% of all new cases of cancer in the United Kingdom (UK) (2016–2018).[2] In addition, breast cancer is the second most common cause of death among females and the fourth most common cause of cancer death in the United Kingdom (2018) accounting for about seven percent of all cancer deaths. In England, about 98% of people with breast cancer who are diagnosed at its earliest stage will live for at least 5 years, compared to about one in four (26%) who are diagnosed at its later stage.[2] The prognosis and overall survival of breast cancer patients are heavily influenced by the presence of axillary lymph node (LN) metastases.[3]

Axillary lymph node dissection (ALND) was the standard procedure for axillary staging for many years, but it has a higher risk of complications.[4] In early stage breast cancer, sentinel lymph node biopsy (SLNB) is currently the gold standard for axillary staging.[5] When compared to complete ALND, the SLNB is associated with significantly fewer complications.[6],[7] In addition to avoiding unnecessary ALND, SLNB aids in determining the number of involved nodes, which is crucial in determining the appropriate postoperative adjuvant treatment. However, it was discovered that other affected LNs in the same region was found in 1 − 15 percent of patients who had a negative sentinel node biopsy for metastases.[8] Large LN metastases in the first drainage node account for the majority of these false negative results.[9]

Axillary ultrasonography represents a cost-effective and noninvasive important technique for the preoperative assessment of axillary node status.[10],[11] Currently, Axillary ultrasonography (AUS) is routinely used for axillary assessment in most European breast cancer units (BCUs).[12] Preoperative axillary staging by ultrasonography (US) may change the management in several ways such as the choice of the operation, the neoadjuvant chemotherapy, etc., However, studies have reported different sensitivity (26%–94%) and specificity (53%–98%) rates for axillary ultrasound.

In the current study, we assessed the diagnostic accuracy of preoperative axillary ultrasonography in breast cancer cases in our clinical setting by comparing the findings with the final histological results obtained during surgery.

  Patients and Methods Top

We carried out this retrospective study in our breast unit for all patients who had breast cancer and axillary surgery, during the period from January 2020 to February 2021. Data were retrospectively collected from the hospital recording system. Inclusion criteria included (1) patients who had breast cancer and axillary staging by preoperative US scan, (2) patients who had either mastectomy or breast conservative surgery, and (3) of any age group. Exclusion criteria included (1) patients with in situ tumor, (2) patients who had neoadjuvant chemotherapy, and (3) patients who did not have any axillary surgery.

All the patients had triple breast assessment in our breast unit. All patients had preoperative axillary assessment by a senior radiologist. General ultrasound machine with breast package was used (Phillip brand) with standard transducer frequency of 18.5 MHz and 12.5 MHz for dense breast tissues. Patients with suspicious LNs during the initial breast assessment, had ultrasound guided tru-cut biopsy. Criteria of suspicious LNs on US included loss of the fatty hilum, irregular appearance of the LN, cortical thickening >3 mm, markedly hypoechoic cortex, and round shape. 14-gauge core-needle were usually used. Biopsy results again were reviewed by a senior pathologist. Results were discussed in our breast multidisciplinary team (MDT) prior to surgery. An informed consent was obtained from every patient before any surgical intervention.

All patient with negative axillary US had SLNB. On the other hand, patients with positive axillary LN as confirmed by US-guided core biopsy had axillary management according to the breast MDT decision. Specimens obtained by either SLNB or axillary dissection were fixed in formalin and sent to the lab for assessment of the number of involved nodes and the degree of involvement (micro or macro-metastasis). Patients with positive axillary LNs again were discussed in our post-operative breast oncology MDT for the assessment of any further axillary management.

The findings from the preoperative axillary US were compared with the results of either SLNB or ALN dissection to assess the diagnostic accuracy of axillary US. Indeterminate LNs on US were included in the same group with the suspicious nodes. We calculated the sensitivity, specificity, positive predictive value, and negative predictive value of AUS based on the final pathology reports.

IRB approval was exempted by our local IRB as all the data was collected retrospectively, fully anonymized, and all images were de-identified.

  Results Top

During the period from January 2020 to February 2021, more than 200 breast operations were performed in our breast surgery department. Our study included 128 patients who met the inclusion and exclusion criteria. Average age of diagnosis was 63.9 ± 12.3 years of age. 63 patients had right-sided breast cancer and 65 had left-sided cancer. Ninety-four patients (73.4%) were diagnosed with invasive ductal carcinoma, 20 patients (15.6%) had invasive lobular carcinoma, while 14 patients (10.9%) had other malignancies including metaplastic carcinoma, tubulolobular carcinoma, mucinous carcinoma, and others. In terms of tumor grading, 16 patients (12.5%) had tumor grade 1, 57 patients (44.5%) had tumor grade 2, and 55 patients (43%) had tumor grade 3. Regarding the tumor size, 46 patients (35.9%) were diagnosed with T1 tumor, 67 (52.3%) with T2, 13 (10.2%) with T3 and 2 (1.6%) with T4 tumor. Receptors status was identified in all our patients and we found that estrogen receptors were positive in 96 patients and negative in 32 patients, while HER2 receptors were positive in 19 patients and negative in 109 patients [Table 1].
Table 1: Patients' demographics

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US was utilized for axillary assessment in all our patients [Figure 1], [Figure 2], [Figure 3], [Figure 4]. We compared the US findings with the final pathology results. US revealed unremarkable findings in 96 patients. The number of true negative patients was 77 (60.2%), while 19 patients (14.8%) were false negative. Of the 19 patients, 15 had macro-metastatic disease and four had micro-metastasis as confirmed with SLNB. The average number of the involved LNs after axillary surgery was two LNs. Of 32 patients who had abnormal LNs on US, true positive patients were 28 (21.9%) and false positive were four patients (3.1%). We calculated sensitivity rate of 59.6%, specificity rate of 95.1%, positive predictive value of 87.5%, and negative predictive value of 80.2% [Table 2] and [Table 3].
Figure 1: US of the left axilla showing normal LN. US: Ultrasonography, LN: Lymph node

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Figure 2: US of the right axilla showing abnormal LNs with cortical thickness of 4.6 mm. US: Ultrasonography, LNs: Lymph nodes

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Figure 3: US of the right axilla showing abnormal LN with cortical thickness of 6.3 mm. US: Ultrasonography, LN: Lymph node

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Figure 4: US of the left axilla showing abnormal LN with cortical thickness of 5.5 mm. US: Ultrasonography, LN: Lymph node

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Table 2: Pathology results compared with ultrasonography results

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Table 3: Sensitivity, specificity, positive predictive value, and negative predictive value of ultrasonography in axillary assessment in breast cancer patients

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  Discussion Top

In the United Kingdom, breast cancer is the most common type of malignancy, causing 15% of all new cases between 2016 and 2018. Breast cancer is the most common cancer among females in the UK, accounting for approximately 55,500 new cases annually. According to the reports, breast cancer is the fourth most common cause of cancer-related death in the United Kingdom, causing seven percent of all cancer-related deaths.[2] Early diagnosis is associated with excellent prognosis as compared with late diagnosis. A significant prognostic factor in patients with invasive breast cancer is the status of their axillary LNs.[3] Preoperative axillary staging was solely based on the physical examination for many years; the sensitivity of physical examination is low (34%–76%).[13] Moreover, physical examination is unable to differentiate between reactive and metastatic LNs.[7]

Currently, patients with breast cancer are routinely evaluated prior to surgery with axillary ultrasound (AUS) in the majority of the BCU.[14] Bruneton et al. compared the diagnostic accuracy of preoperative axillary ultrasound with palpation in the detection of nodal metastasis in breast cancer and reported that US had sensitivity and specificity rates of 72.7% and 97.3%, respectively, whereas palpation had sensitivity and specificity rates of only 45.4% and 97.3%, respectively.[15] US is noninvasive, widely available and inexpensive diagnostic technique. It can also evaluate the morphological characteristics of LNs that are palpable and those that aren't. Loss of the fatty hilum, cortical thickening >3 mm, irregular shape, markedly hypoechoic cortex, round shape, and increased peripheral blood flow were ultrasound findings that raised the possibility of axillary metastasis.[16],[17],[18] The morphology and cortical thickness, according to many authors, are the most crucial parameters for determining metastatic LNs[17],[19],[28] [Figure 1], [Figure 2], [Figure 3], [Figure 4].

Different studies reported variable sensitivity and specificity rates for AUS; Bonnema et al., reported sensitivity rate of 87% and specificity rate of 56%,[21] Podkrajsek et al., in a study including 165 patients published a sensitivity and specificity rates for AUS of 58% and 89%, respectively.[22] Moreover, Nori et al. concluded a sensitivity rate of 45.2%, a specificity rate of 86.8%, with a positive predictive value of 61.3% and negative predictive value of 77.2%.[23] The variability in the sensitivity and specificity rates may be attributed to many factors. The use of different sonographic criteria for evaluating axillary LNs and the radiographer's experience levels may contribute to this wide variation.[19],[24] Furthermore, Dihge et al. determined an association between the accuracy of AUS with the metastatic size (odds ratio [OR] = 1.11), obesity (OR = 2.46), and histological grade (OR = 4.43),[25] and concluded that the variable sensitivity and specificity rates may also be influenced by the tumor type and LN size,[26] as well as patients' characteristics like obesity, which may limit the detection of axillary LN involvement due to the fat mass.[27] Other factors that may contribute to the variable rates in sensitivity and specificity include the difference in the equipment and transducer frequencies used. In addition, sentinel node biopsy may result in verification bias due to false-negative results.[19]

In our study, AUS was performed by at least a senior radiologist. All patients with breast cancer had US assessment of the axilla regardless of the axillary clinical evaluation. We could not evaluate the body mass index for every patient as it was retrospective review and not all these data were well documented in the patients' notes.

Patients with in situ carcinoma were excluded from the study. 88.3% of our patients had early-stage breast cancer (T1 and T2). All patients were discussed in breast MDT. Patients with negative axillary examination on US were subjected to SLNB. Final histology results were compared with the US findings. True positive, false positive, true negative, and false-negative values were identified. We concluded sensitivity rate of 59.6%, specificity rate of 95.1%, positive predictive value of 87.5%, and negative predictive value of 80.2, with an overall accuracy rate of 82.2%. Our accuracy rate was higher than figures published by Kochler et al., and Nori et al.[20],[23]

Numerous factors may have contributed to the false negative results in our study including patients' factors like obesity and the degree of shoulder movement. The radiographer's level of experience could also be a significant factor. The size of the LNs as well as the type and grade of the tumor may have an impact on the outcomes.

To improve the results of AUS, US-guided biopsy of the axillary nodes has been introduced. The indications for needle biopsy were different between different studies. Although in some studies only abnormal looking LNs on US were biopsied,[13],[29],[30],[31] in other studies, all nodes were biopsied regardless of its size or appearance on sonography.[21],[32],[33] The use of US-guided biopsy has increased the specificity rate, which reached as high as 100%; however, the sensitivity rate was reduced. Core biopsy was found to be more sensitive than fine-needle aspiration in detecting metastasis, according to some studies.[34],[35] In our study, all abnormal looking LNs on US scan, were biopsied. Ultrasound-guided core biopsy was the standard procedure in our patients for the assessment of any abnormal looking LN. Of all suspicious criteria, increased cortical thickness and loss of the fatty hilum were the most common indicators for biopsy. Thirty-two patients with abnormal looking nodes on US had US-guided core biopsy; four of them did not have any metastatic disease as confirmed also after the SLNB.

The results of our study may have some limitations. First, the number of the included patients was relatively small (128 patients). Second, the level of experience of the radiologist performing the AUS or the variability of the ultrasound device could have affected the results. Third, we could not compare the LN characteristics with the intraoperative pathological findings.

  Conclusion Top

Although US is a useful technique for axillary staging in breast cancer patients, it should not be used to definitively identify axillary lymph involvement. Many factors may contribute to the variable sensitivity and specificity rates of US between different centers. To improve the diagnostic accuracy of US, additional studies with a larger population and intra-operative US would be recommended for comparison of the characteristics of each LN detected with pathological finding of the same LN.

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Conflicts of interest

There are no conflicts of interest.

  References Top

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Correspondence Address:
Emad Mofid Nassif Rezkallah,
Voyager House 201, James Cook Accommodation, Marton Road, Middlesbrough, TS4 3BW
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Source of Support: None, Conflict of Interest: None


  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1], [Table 2], [Table 3]


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