Targeted axillary dissection in breast cancer patients with metastatic nodal disease: a prospective study on localization techniques and oncological outcomes
Original Article

Targeted axillary dissection in breast cancer patients with metastatic nodal disease: a prospective study on localization techniques and oncological outcomes

Geok Hoon Lim1,2, Aisha Masoud Al Shukairi1, Yien Sien Lee3, Sze Yiun Teo3, Zhiyan Yan1, Qing Ting Tan1, Mihir Gudi4, Ruey Pyng Ng5, Fuh Yong Wong6

1Breast Department, KK Women’s and Children’s Hospital, Singapore, Singapore; 2Duke-NUS Medical School, Singapore, Singapore; 3Department of Diagnostic and Interventional Imaging, KK Women’s and Children’s Hospital, Singapore, Singapore; 4Department of Pathology and Laboratory Medicine, KK Women’s and Children’s Hospital, Singapore, Singapore; 5Division of Nursing, KK Women’s and Children’s Hospital, Singapore, Singapore; 6Division of Radiation Oncology, National Cancer Centre, Singapore, Singapore

Contributions: (I) Conception and design: GH Lim; (II) Administrative support: RP Ng; (III) Provision of study materials or patients: GH Lim, QT Tan, Z Yan, FY Wong; (IV) Collection and assembly of data: AM Al Shukairi, GH Lim, FY Wong; (V) Data analysis and interpretation: All authors; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Geok Hoon Lim, MBBS, FRCS. Breast Department, KK Women’s and Children’s Hospital, 100 Bukit Timah Road, Singapore 229899, Singapore; Duke-NUS Medical School, 8 College Road, Singapore 169857, Singapore. Email: ghlimsg@yahoo.com.sg.

Background: Neoadjuvant chemotherapy followed by targeted axillary dissection (TAD) has been proposed as an alternative to axillary lymph node dissection (ALND) in breast cancer patients with metastatic nodal disease. However, there is lack of standardization of TAD technique. This study aimed to prospectively evaluate the effectiveness of various localization techniques in TAD and assess the oncological outcomes of TAD alone versus ALND.

Methods: Breast cancer patients with histologically proven nodal metastasis (T1-4N1-2M0) and neoadjuvant chemotherapy were included. Patients were divided into three groups: TAD-alone, TAD with ALND, and upfront ALND. Localization techniques used during TAD were assessed and oncological outcomes were compared between the TAD alone and ALND groups. This study was registered with ClinicalTrials.gov (identifier: NCT03878017).

Results: One hundred and twenty-three patients, of which 18, 18, 87 underwent TAD alone, TAD with ALND and upfront ALND respectively, were included. All localization techniques, such as skin marking, Savi Scout and radio-guided occult lesion localization (ROLL) resulted in 100% retrieval of the marked node. Single-agent sentinel node localization during TAD was feasible. After a median follow-up of 13 and 23 months for the TAD-alone and ALND groups respectively, there were no significant differences in their oncological outcomes.

Conclusions: Various localization techniques, including the less studied skin marking and ROLL, were effective in TAD. During TAD, single agent may be used for sentinel node localization. TAD alone did not have inferior oncologic outcomes on short term follow-up and may replace ALND in patients with complete nodal pathological response after neoadjuvant chemotherapy. Our findings need validation in larger studies with longer follow-up.

Keywords: Breast cancer; axillary lymph node dissection (ALND); targeted axillary lymph node dissection (targeted ALND); survival; sentinel lymph node biopsy (SLNB)


Submitted Apr 21, 2025. Accepted for publication Jul 07, 2025. Published online Aug 20, 2025.

doi: 10.21037/gs-2025-166


Highlight box

Key findings

• Various localization techniques, including the less studied skin marking and radio-guided occult lesion localization (ROLL), were effective in targeted axillary dissection (TAD).

• During TAD, single agent may be used for sentinel node localization.

• TAD alone did not have inferior oncologic outcomes on short term follow-up.

What is known and what is new?

• Neoadjuvant chemotherapy followed by TAD has been proposed as an alternative to axillary lymph node dissection (ALND) in breast cancer patients with metastatic nodal disease. However, there is lack of standardization of TAD technique.

• This study prospectively evaluated the effectiveness of various localization techniques in TAD and assessed the oncological outcomes of TAD alone versus ALND.

What is the implication, and what should change now?

• TAD may replace ALND in patients with complete nodal pathological response after neoadjuvant chemotherapy. Our findings need validation in larger studies with longer follow-up.


Introduction

In breast cancer patients with metastatic nodal disease, neoadjuvant chemotherapy could be given to avoid axillary lymph node dissection (ALND) in patients with a good response. This is especially true in patients with unfavorable subtypes, such as the triple negative (1) or human epidermal growth factor receptor 2 (HER2) positive patients (2), whereby a nodal pathological complete response (PCR) of 40% to 75% could be achieved (3).

Targeted axillary dissection (TAD) has been proposed as one of the ways to assess the axillary status of the patient after neoadjuvant chemotherapy. However, there is no standardization of TAD with a variety of localizing agents being used for the localization of the marked node (4). Various localization techniques have been described, namely the wire, Savi Scout radar localization, magnetic seed, radioactive seed, charcoal tattooing, skin marking and radio-guided occult lesion localization (ROLL) placement etc. (5-11).

Besides the variation of localization agents, it remained unclear how many sentinel lymph nodes should be harvested during TAD (12). Also, it remained unknown if the use of single agent for sentinel lymph node biopsy (SLNB) during TAD would affect the accuracy of TAD. While the diagnostic efficacy of various localizing agents in TAD has been demonstrated (13), there remained scarce data on the oncological outcomes following TAD alone in patients who had initially metastatic nodal disease and now achieved ypN0. It remained controversial too if patients with initially more than three radiologically abnormal lymph nodes and good response after neoadjuvant chemotherapy would benefit from TAD alone.

We aimed to prospectively evaluate the effectiveness of some of the less reported methods for the localization of the marked node during TAD, while assessing if the inclusion of patients with initially more than three radiologically abnormal lymph nodes and using single agent for SLNB identification could affect the oncological outcomes of the patients with TAD alone. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-166/rc).


Methods

Design and setting

Breast cancer patients who underwent TAD at KK Women’s and Children’s Hospital, Singapore between 1 June 2020 and 31 July 2024 were recruited prospectively. The group of patients who underwent TAD without ALND was compared to a cohort during the same period who had ALND, either due to metastatic lymph node during TAD or as an upfront surgery. The data of the latter group was obtained from a prospectively kept database.

Participants

Female patients aged 18 years old or older who were diagnosed to have invasive breast cancer with histologically proven metastatic axillary node were included. We excluded patients who were genetic mutation carriers, pregnant, stage IV disease and patients with synchronous or metachronous bilateral breast cancers.

For patients undergoing TAD, they had marking of the biopsied proven metastatic lymph node prior to neoadjuvant chemotherapy which was anthracycline and/or taxane based. Neoadjuvant chemotherapy was offered to patients with nodal metastasis and unfavorable subtypes such as triple negative or HER2 positive patients. For patients with estrogen receptor (ER) positive and HER2 negative subtype, neoadjuvant chemotherapy was offered for premenopausal patients who had metastatic nodal disease or patients who had locally advanced disease. HER2 targeted therapy was added, depending on HER2 positivity. After neoadjuvant chemotherapy, the patient underwent operation.

TAD was performed primarily by three surgeons. During TAD, localization of the marked node was done using a variety of methods depending on the surgeons’ preference. These methods included skin marking, Savi scout radar localization, ROLL, etc. Skin marking technique was previously described (10) and essentially involved inserting an ultrasound visible clip into the metastatic lymph node prior to neoadjuvant chemotherapy. After neoadjuvant chemotherapy, this clip was identified by performing an axillary ultrasound, with the patient’s ipsilateral arm being positioned in the operative position. A marking is then placed on the skin directly above the clip and the clipped node was then localized based on this marking and removed. This technique avoids the use of an expensive localizer but was only suited for superficial clipped nodes. ROLL technique involved the injection of the clipped node with radioisotope which then aided the identification and removal of the clipped node.

SLNB identification during TAD was performed using single or dual agents based on the surgeons’ preference. If dual tracers were used, they were blue dye and radioisotope. Intra-operative confirmation of excision of the marked node was attained with specimen radiography. ALND was performed when there was metastasis of the lymph node reported on frozen section of the nodes retrieved during TAD.

Following surgery, the patients were managed based on the recommendations following a multidisciplinary team meeting.

Data obtained included demographic, radiological and pathological features. Treatment details and oncological outcomes were obtained too. In this paper, nodal irradiation was defined as the receipt of axillary and/or supraclavicular radiation. The outcomes were reviewed to determine if the variations of TAD localization affected the clinical outcomes and to compare the rate of recurrence and survival in patients with TAD alone versus patients with ALND.

Statistical analysis

Categorical variables were expressed using frequencies and percentages, whereas continuous variables were expressed with mean and range. Categorical variables were compared using Fisher’s exact tests whereas continuous variables were compared using t-test. The confidence intervals (CIs) were set at 95% with P value being significant if it was <0.05. Statistical analysis was carried out using GraphPad statistical software (version 2025).

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by SingHealth Centralised Institutional Review Board (CIRB Ref. 2020/2828 and 2019/2419). Patients who were recruited prospectively signed informed consent, whereas consent was waived for patients who did not undergo TAD.

This study was registered with ClinicalTrials.gov (identifier: NCT03878017).


Results

One hundred and twenty-three patients were included, with 18, 18, 87 patients undergoing TAD alone, TAD with ALND and upfront ALND, respectively. The median age of the patients who had TAD alone versus ALND was 50 (range, 33–67) and 53 (range, 29–77) years old, respectively.

Most of the patients had invasive ductal carcinoma (Table 1). Both groups had similar baseline tumor size measured on ultrasound prior to neoadjuvant chemotherapy, with a mean of 39.6 (range, 14–110) and 42.9 (range, 10–163) mm for the TAD-alone and ALND groups, respectively. A median of 1 (range, 1–5) and 2 (range, 1–7) suspicious lymph nodes were seen at baseline axillary ultrasound in the TAD-alone versus ALND groups, respectively. The median number of lymph nodes harvested in the TAD-alone group was 4 (range, 1–7) versus 15 (range, 1–36) in the ALND group. Overall nodal PCR rate was 59.3%.

Table 1

Characteristics of patients who underwent TAD alone versus ALND after neoadjuvant chemotherapy

Characteristics Patients with TAD alone (N=18) Patients with ALND (N=105) P value
Clinical features
   Age (years) 0.30
    ≤50 9 (50.0) 38 (36.2)
    >50 9 (50.0) 67 (63.8)
   BMI (kg/m2) 0.11
    <18.5 3 (16.7) 5 (4.8)
    18.5–24.9 7 (38.9) 50 (47.6)
    25–29.9 7 (38.9) 29 (27.6)
    ≥30 1 (5.5) 21 (20.0)
Sonographic features
   Breast tumour size (mm) >0.99
    ≤20 2 (11.1) 16 (15.2)
    >20 to ≤50 12 (66.6) 64 (61.0)
    >50 4 (22.2) 25 (23.8)
Pathological features
   Breast tumour histology >0.99
    Invasive ductal 17 (94.4) 93 (88.6)
    Invasive lobular 1 (5.5) 8 (7.6)
    Others 0 4 (3.8)
   Grade 0.11
      I 0 4 (4.0)
      II 5 (31.3) 55 (55.6)
      III 11 (68.7) 40 (40.4)
      Missing 2 6
   ER 0.08
    Positive 7 (38.8) 65 (61.9)
    Negative 11(61.1) 40 (38.1)
   PR 0.02
    Positive 4 (22.2) 57 (54.3)
    Negative 14 (77.7) 48 (45.7)
   HER2 0.43
    Positive 13 (72.2) 62 (59.0)
    Negative 5 (27.7) 43 (41.0)
   ypT 0.03
     ypTpcr 12 (66.6) 37 (35.2)
     ypT1 6 (33.3) 41 (39.0)
    ypT2 0 21 (20.0)
    ypT3 0 6 (5.7)
    ypT4 0 0
   ypN 0.001
    ypN0 18 (100.0) 55 (52.4)
    ypN1 0 31 (29.5)
    ypN2 0 11 (10.5)
    ypN3 0 8 (7.6)
Surgical management of the breast <0.001
   Mastectomy 6 (33.3) 84 (80.0)
   Breast conservation 12 (66.6) 21 (20.0)
Adjuvant radiotherapy 0.69
   Yes 16 (88.9) 94 (90.4)
   No 2 (11.1) 10 (9.6)
   Missing 0 1
Nodal irradiation (axilla and/or supraclavicular radiation) 0.07
   Yes 12 (66.6) 43 (41.3)
   No 6 (33.3) 61 (58.7)
   Missing 0 1
Ipsilateral axillary recurrence >0.99
   Yes 0 1 (1.0)
   No 18 (100.0) 104 (99.0)
Distant metastasis >0.99
   Yes 1 (5.5) 5 (4.8)
   No 17 (94.5) 100 (95.2)
Breast cancer related mortality 0.55
   Yes 1 (5.5) 4 (3.8)
   No 17 (94.5) 101 (96.2)

Data are presented as No. (%). , if multifocal/centric disease was present sonographically, the breast size measurement will be based on the largest size of all lesions; , based on biopsy result. ALND, axillary lymph node dissection; BMI, body mass index; ER, estrogen receptor; HER2, human epidermal growth factor receptor 2; PR, progesterone receptor; TAD, targeted axillary dissection.

Of the patients who underwent TAD, 19, 9, and 8 had Savi Scout, ROLL and skin marking, respectively, for localization of the marked node (Table 2). All localization techniques resulted in successful retrieval of the marked nodes in 100% of cases. The metastatic node was detected via the marked node in 94.4% of cases. Single agent (blue dye) was used for the identification of SLN during TAD in one case and this did not affect the accuracy of TAD.

Table 2

Localization characteristics of patients with TAD

TAD characteristics Patients with TAD alone (N=18) Patients with TAD and ALND (N=18)
Clipped node identification
   Savi scout 10 (55.6) 9 (50.0)
   ROLL 6 (33.3) 3 (16.7)
   Skin marking 2 (11.1) 6 (33.3)
Success in clipped node retrieval
   Yes 18 (100.0) 18 (100.0)
   No 0 0
Sentinel lymph node identification during TAD
   Single technique 0 1 (5.6)
   Dual technique 18 (100.0) 17 (94.4)
Metastatic node detected via clipped node
   Yes 17 (94.4)
   No 1 (5.6)

Data are presented as No. (%). ALND, axillary lymph node dissection; ROLL, radio-guided occult lesion localization; TAD, targeted axillary dissection.

On statistical analysis, progesterone receptor (PR) negativity was more prevalent in the TAD-alone group compared to the ALND group (P=0.02). A total of 66.6% of patients in the TAD alone and 35.2% of patients in the ALND group achieved complete pathological response of the tumor in the breast respectively (P=0.03). More patients in the TAD-alone group underwent breast conservation, whereas the majority of patients with ALND underwent mastectomy (P<0.001). Not surprisingly, the TAD-alone group had a higher prevalence of ypN0 compared to the ALND group (P=0.001), though 52.4% of ALND patients achieved ypN0.

There were, however, no statistical differences in the ipsilateral axillary recurrence or breast cancer related mortality rates between the two groups, after a median follow-up of 13 and 23 months respectively for the TAD-alone and ALND groups.


Discussion

This study prospectively demonstrated the use of various localization methods for the marked metastatic node, coupled with variations in SLNB identification technique during TAD. The various localization techniques all resulted in successful retrieval of the marked node and the marked node was an accurate predictor of the axillary status. Use of a single agent for SLNB identification during TAD was feasible too and did not seem to impair the accuracy of TAD. Despite the variations in performing TAD in patients, TAD alone did not result in a worse oncological outcome compared to ALND on short term follow-up.

Since the introduction of TAD, various localization methods of the marked metastatic node, including wire and wire-free (14) techniques, have been described. These various localization techniques were safe, feasible and accurate, though each technique has its own pros and cons (15). In this paper, we also studied localization methods which were less reported in literature, such as the skin marking technique (10) and the ROLL technique, and proved that they were effective in the localization of the marked node. The skin marking technique, which is suitable for patients with superficial lymph nodes, has the advantage of being simple to perform, non-invasive and could avoid the cost of a localization agent.

TAD comprised of localization of the metastatic node and SLNB. However, the number and mode of SLNB identification during TAD has not been well studied. Using dual agent for the identification of SLNB in the adjuvant setting remained the gold standard with detection rates often exceeding 98% and a false-negative rate below 5% (16). In a systematic review (17), using blue dye alone resulted in a lower detection rate of around 91% and a false-negative rate of around 13%. However, it remained a valuable and fairly accurate way of assessing the axillary status, especially in resources limited areas with no radioisotope access (18-21). Despite the lower detection rate with blue dye alone, its prediction of the axillary nodal status was comparable to that of radioisotope alone or dual agent (radioisotope and blue dye) localization (22). Conversely, using radioisotope alone, the detection rate was typically higher than blue dye at around 96%, with a lower false-negative rate (23). In patients with metastatic lymph nodes and attempting a trial of axillary preservation after neoadjuvant chemotherapy, SLNB alone could be attempted. However, in these cases, dual agents were needed for the identification of the SLNB and at least three nodes had to be harvested to achieve an acceptable false negative rate (24). In the neoadjuvant setting, retrieval of the marked node alone can be associated with a low false negative rate of 7% (25). In a systematic review, though the addition of SLNB could reduce the false negative rate from 6.28% (26) in patients with marked node removal alone to 5.18%, this difference was not statistically significant. Hence, the number of SLN that should be harvested during TAD remained unknown though it had been reported to be lower (27) compared to using SLNB alone for a trial of axillary preservation. It remained unclear also if having few SLN being harvested during TAD would impact the patient clinically. In addition, a single agent technique for identification of the SLNB during TAD may suffice based on our findings, though it was a small sample size. These above findings, however, need validation in future studies.

In our study, PR status was found to be statistically different between patients who underwent TAD alone compared to those who had ALND, with the former group having a higher frequency of patients with PR negativity. This finding was also demonstrated in other studies which reported that PR negativity in patients with ER positive and HER2-negative subtype could improve nodal PCR rate (28,29).

Breast PCR (ypTpcr) has been reported to be associated with ypN0 (30), which was also demonstrated in our study. More patients underwent a mastectomy in the ALND group compared to patients in the TAD-alone group. Several factors could account for this including a larger tumor to breast size ratio, multicentric tumor or the patient’s preference for mastectomy (31). Nonetheless, breast conservation remained a safe option which has comparable survival as mastectomy (32) after neoadjuvant chemotherapy. Hence, despite a difference in the prevalence of surgical techniques between the TAD-alone and ALND groups, this factor was unlikely to affect the oncological outcomes between the two groups, since the tumour size of both groups remained comparable.

Like other studies (33,34), our study did not show an inferior oncological outcome in patients who underwent TAD alone compared to patients with ALND. A recent prospective study (35) also showed comparable oncological outcomes in patients with TAD and ALND versus TAD alone when at least 3 lymph nodes were harvested during TAD. However, the use of TAD in patients with initially more than 3 radiologically abnormal lymph nodes (36) remained unclear. Unique to our study, we included patients with >3 abnormal lymph nodes seen on axillary ultrasound, in all molecular subtypes, for consideration of TAD and despite the heavier nodal burden, the oncological outcomes in patients with TAD alone were comparable to patients with ALND.

Strengths of this study included validation of less reported localization techniques such as skin marking. It also explored the feasibility of the use of a single agent for identification of the SLN during TAD which was not well studied. As our breast imaging unit would routinely document the number of abnormal lymph nodes seen on axillary ultrasound, this allowed us to correlate oncological outcomes in the group of patients with initially more than three radiologically abnormal lymph nodes. Being a prospective study, there was little missing data.

However, our study was not without limitations which included a small sample size of patients with TAD alone since this is a study reporting our initial experience with this newly introduced technique. Follow-up for this group of patients was short as well, since the study started recruitment only in 2020. Though promising results were demonstrated in our study, larger studies with longer follow-up duration are needed to validate our findings.


Conclusions

In conclusion, various methods can be used for the localization of the marked node during TAD. Use of a single agent for SLN identification during TAD may be feasible. In this group of patients with histologically proven metastatic disease and initially multiple abnormal lymph nodes radiologically, the oncological outcomes were comparable between the patients with TAD alone versus ALND on short-term follow-up. Further larger studies with collaboration with other centers and longer follow-up would be needed for validation of the results.


Acknowledgments

None.


Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-166/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-166/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-166/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-166/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by SingHealth Centralised Institutional Review Board (CIRB Ref. 2020/2828 and 2019/2419). Patients who were recruited prospectively signed informed consent whereas consent was waived for patients who did not undergo TAD.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.


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Cite this article as: Lim GH, Al Shukairi AM, Lee YS, Teo SY, Yan Z, Tan QT, Gudi M, Ng RP, Wong FY. Targeted axillary dissection in breast cancer patients with metastatic nodal disease: a prospective study on localization techniques and oncological outcomes. Gland Surg 2025;14(8):1529-1538. doi: 10.21037/gs-2025-166

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