10-Year Outcomes of Targeted Axillary Surgery after Neoadjuvant Chemotherapy in Breast Cancer

doi:10.21203/rs.3.rs-5004479/v1

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10-Year Outcomes of Targeted Axillary Surgery after Neoadjuvant Chemotherapy in Breast Cancer

https://doi.org/10.21203/rs.3.rs-5004479/v1

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Background: When pathological complete response (pCR) after neoadjuvant chemotherapy (NAC) is achieved, identifying traces of the previous tumor site or lymph nodes and performing accurate surgery becomes challenging. We conducted ultrasound-guided targeted axillary surgery (TAS) in patients with node-positive breast cancer treated with NAC. Survival outcomes were compared with those of patients who underwent conventional axillary lymph node dissection (ALND).

Methods: We conducted a retrospective analysis of 235 patients (TAS, n=78; ALND, n=157) with cT1-3N1-2 breast cancer who underwent NAC followed by surgery from 2012 to 2017. Patients were treated with standard treatments, and oncologic results, including locoregional recurrence-free survival, distant metastasis-free survival, and overall survival (OS), were assessed over a 10-year follow-up period.

Results: There was no significant difference in oncologic outcomes between two groups and based on subtypes, including hormone receptor (HR)-positive, HER2-positive, and triple-negative breast cancer (TNBC). In the HR-positive breast cancer group, the TAS and ALND groups showed very similar trends . In HER2-positive breast cancer, although not statistically significant, the survival outcomes were better in the TAS group than in the ALND group. However, the OS in the TAS group for TNBC was lower than that in the ALND group, though not significantly.

Conclusions and Relevance: This study demonstrates that TAS is comparable to ALND in terms of 10-year oncological outcomes across different types of node-positive breast cancer, suggesting its potential as a viable alternative.

Breast cancer

Node metastasis

Neoadjuvant chemotherapy

Targeted axillary sampling

According to the NCCN guidelines, clinically node-positive breast cancer can be treated using neoadjuvant chemotherapy (NAC)¹. Treatment responses to NAC vary according to the breast cancer subtype, with HER2-positive and triple-negative breast cancer (TNBC) exhibiting substantially higher responses than hormone-positive breast cancer^2–5. Because the prognosis of patients who show a pathologic complete response (pCR) has been reported to be considerably better than that of those who show a non-pCR, the goal of NAC is to achieve a pCR for breast cancer^6,7.

It is essential that the primary tumor bed be pathologically evaluated to verify whether pCR has been achieved. To not miss the exact primary tumor site, various techniques have been established to track cancer and confirm that the region has been accurately excised^8–12. Since 2000, the most common method for monitoring breast cancer has been placing a clip in the center of tumor^13,14. After removing the breast tissue, it is essential to confirm whether the clip was successfully removed by intraoperative specimen mammography. A tattooing method using dyes such as activated charcoal has also been used for the accurate resection of breast cancer or axillary lymph nodes^15,16, and marking axillary lymph nodes with the radioactive iodine ¹²⁵I Seeds (MARI) technique with placement of a radioactive seed into a positive lymph node is also one of these tracking procedures^17–19. The false-negative rate of these methods has been reported to be 7–20%.

In prior studies, our team validated the targeting feasibility using the activated charcoal tattooing technique or clip placement at diagnosis in patients with breast cancer who received NAC^20,21. This approach was also applied to patients who underwent upfront surgery with targeted axillary surgery (TAS), and the 5-year oncological outcomes have been reported²². Herein, we update the oncologic outcomes with a 10-year follow-up period of patients with cT1-3N1-2 breast cancer who underwent NAC followed by TAS surgery.

Between 2012 and 2017, a total of 1,984 female patients with operable breast cancer who were treated at Kyungpook National University Chilgok Hospital were reviewed. All patients were diagnosed with invasive breast cancer by needle or excision biopsy, and axillary lymph node metastasis was confirmed by fine-needle aspiration cytology or needle biopsy. Breast cancer and metastatic axillary lymph nodes were assessed according to their size, location, and number based on mammography, ultrasonography, and breast magnetic resonance (MR) imaging before treatment. Patients who received upfront surgery for NAC (n = 1,572) and those who underwent sentinel lymph node biopsy after NAC (n = 125) were excluded. A total of 235 patients with cT1-3N1-2 breast cancer provided written informed consent to undergo breast surgery and axillary surgery (TAS, n = 109; ALND, n = 127), and 30 patients who underwent initial TAS and then ALND were classified into the ALND group. Finally, 78 patients were classified as the TAS group, and 157 patients were classified as the ALND group. After surgery, the standard adjuvant treatment was completed, and surveillance was performed biannually for the first 2 years and annually thereafter for a further 8 years. Routine surveillance was conducted using blood tests, tumor markers, mammography, breast ultrasonography and MR imaging, chest and abdominal CT, and bone scans (Fig. 1).

For the TAS procedure, targeted techniques for axillary lymph nodes were conducted by ultrasound with tattooing using Charcotrace black ink (Phebra, Lane Cove West, Australia) and by clip insertion for the accurate resection of the lymph node. While 1–3 mL of Charcotrace was injected using a 23-gauge needle into the adjacent soft tissue after local anesthesia for tattooing, a clip (UltraClip® Breast Tissue Markers, BARD NJ, USA) was inserted into the center of the lymph node^20,21. Whether the procedure was performed or not, the patients underwent breast-conserving surgery or mastectomy for the complete removal of the breast cancer. Axillary surgery was performed as either ALND or TAS, depending on the patients’ decision, and the final plan was determined by surgeons before and during the surgery. The patients receiving the TAS were informed that they would need to receive additional radiotherapy in the axillary region. The TAS procedure was performed by leaving sufficient soft and lymphoid tissue around the axillary vessels based on the definition of the surgical boundaries, and ALND was performed using the conventional technique²².

The clinical variables assessed, including age at diagnosis, body mass index (BMI), type of tumor, clinical and pathologic tumor size, type of surgery, number of total and metastatic axillary lymph nodes, tumor subtypes, and additional treatments, were retrospectively reviewed based on the patient’s medical records. The molecular breast cancer subtypes were classified based on the results of immunohistochemical staining of the biopsy samples before the initial treatment as either hormone receptor (HR) positive breast cancer [either estrogen receptor (ER) or progesterone receptor (PR) is positive], HER2-positive breast cancer (ER and PR are negative; HER2 gene is positive), or TNBC (ER, PR, and HER2 are all negative). The Ki67 index was considered high when > 15% of the tumor cells showed nuclear immunoreactivity. The ASCO/CAP 2016 guidelines were followed for the histopathological examination of the four biomarkers.

Statistical analysis for oncologic results was assessed using the locoregional recurrence-free survival (LRFS), distant metastasis-free survival (DMFS), and overall survival (OS) parameters using SPSS version 29.0 (SPSS, Chicago, IL, USA). For the comparison of ALND versus TAS with axillary radiotherapy, categorical or continuous variables were evaluated using the χ² test or Student’s t-test, and oncologic outcomes, including locoregional recurrence, distant metastasis, and death, were assessed with Kaplan-Meier analysis. P < 0.05 was defined as statistically significant.

The mean age of the 235 patients was 48.2 years (standard deviation (SD), ± 9.7 years), and the mean BMI was 24.6 kg/m² (SD, ± 3.9 kg/m²). The most common tumor type was invasive ductal carcinoma in both groups (TAS, 96.2%; ALND, 100.0%) (p < 0.001). Although the clinical tumor size was significantly larger in the ALND group (p = 0.003), there were no statistical differences in the clinical T stage or number of suspicious axillary lymph nodes at diagnosis (p = 0.062 and p = 0.985, respectively). Breast-conserving surgery was frequently performed in the TAS group (p < 0.001), and 10 patients in the TAS group did not receive axillary radiotherapy (Table 1).

Table 1

Clinical characteristics of patients with breast cancer who underwent neoadjuvant chemotherapy followed by targeted axillary surgery or axillary lymph node dissection
		Targeted axillary surgery (n = 78)	Axillary lymph node dissection (n = 157)	p-value
Age (mean ± SD, years)		49.2 ± 10.2	47.8 ± 9.5	0.345
Body mass index (mean ± SD, kg/m²)		24.8 ± 3.8	24.5 ± 4.0	0.621
Menopausal status	Pre-menopause	41 (52.6)	113 (72.0)	0.022
	Post-menopause	37 (47.4)	44 (28.0)
Type of tumor (n, %)	Invasive ductal carcinoma	75 (96.2)	157 (100.0)	< 0.001
	Invasive lobular carcinoma	2 (2.6)	0 (0.0)
	Mixed invasive ductal and lobular carcinoma	1 (1.3)	0 (0.0)
Clinical tumor size (mean ± SD, cm)		3.9 ± 1.9	5.1 ± 2.5	0.003
Clinical T stage	T1	8 (10.3)	9 (5.7)	0.062
	T2	54 (69.2)	96 (61.1)
	T3	16 (20.5)	52 (33.1)
No. of suspicious axillary lymph nodes	1–3	46 (59.0)	82 (52.3)	0.985
	4–9	27 (34.6)	66 (42.0)
	> 10	5 (6.4)	9 (5.7)
Type of breast surgery (n, %)	Breast-conserving surgery	31 (39.7)	11 (7.0)	< 0.001
	Mastectomy	47 (60.3)	146 (93.0)
Regimen of neoadjuvant chemotherapy (n, %)	Anthracycline/Cyclophosphamide (AC)	3 (3.8)	6 (3.8)	-
	Sequential AC and Taxane ± Target therapy	60 (76.9)	141 (89.8)
	Docetaxel/Carboplatin + Target therapy	12 (15.4)	9 (5.7)
	Others	3 (3.8)	1 (0.6)
Adjuvant chemotherapy (n, %)		1 (1.3)	3 (1.9)	< 0.001
Adjuvant radiotherapy (n, %)	Breast	74 (94.9)	142 (90.4)	0.119
	Axillary area	68 (87.2)	41 (26.1)	0.008
Adjuvant hormonal therapy (n, %)		54 (69.2)	108 (68.8)	0.891
SD, standard deviation

After NAC, the pathologic tumor size was significantly smaller in the TAS group (p < 0.001), and the pCR rate of the breast and axillary area was significantly higher in the TAS group (p < 0.001 and p < 0.002, respectively). The distribution of the breast tumor subtypes was not different between the two groups. In the TAS group, HR-positive breast cancer was present in 51 cases (65.4%), HER2-positive breast cancer in 10 cases (12.8%), and TNBC in 17 cases (21.8%). In the ALND group, HR-positive breast cancer was present in 107 cases (68.2%), HER2-positive breast cancer in 21 cases (36.8%), and TNBC was found in 29 cases (18.5%). All subtypes were not different between the two groups (Table 2).

Table 2

Pathologic characteristics of patients with breast cancer who underwent neoadjuvant chemotherapy followed by targeted axillary surgery or axillary lymph nodes dissection
		Targeted axillary surgery (n = 78)	Axillary lymph node dissection (n = 157)	p-value
Rate of pathologic complete response (pCR) (n, %)	Breast	25 (32.1)	20 (12.7)	< 0.001
	Axillary lymph nodes	52 (66.7)	68 (43.3)	0.002
Pathologic tumor size (mean ± SD, cm)		1.0 ± 1.3	1.9 ± 2.1	< 0.001
No. of metastatic lymph nodes (mean ± SD)		1.6 ± 0.9	2.7 ± 4.6	0.021
No. of removed lymph nodes (mean ± SD)		8.5 ± 3.6	14.1 ± 8.3	< 0.001
Estrogen receptor (n, %)	Positive	43 (55.1)	79 (50.3)	0.074
	Negative	35 (44.9)	78 (49.7)
Progesterone receptor (n, %)	Positive	39 (50.0)	76 (48.4)	0.078
	Negative	39 (50.0)	81 (51.6)
c-erbB2 gene (n, %)	Positive	27 (34.6)	50 (31.8)	0.653
	Negative	51 (65.4)	107 (68.2)
Triple-negative breast cancer (n, %)	Positive	17 (21.8)	29 (18.5)	0.667
	Negative	61 (78.2)	128 (81.5)
SD, standard deviation

The follow-up periods of both groups were 98.7 months (SD, ± 16.4 months) in the TAS group and 109.2 months (SD, ± 27.3 months) in the ALND group (p = 0.875). There were 25 cases (10.6%) of locoregional recurrence and 42 cases (17.9%) of distant metastasis in the patients. There was no statistical difference in the LRFS and DMFS between the TAS and ALND groups (p = 0.673 and p = 0.729, respectively). The OS was also similar in both groups (p = 0.396) (Fig. 2). There were 7 (9.0%) and 18 (11.5%) cases of locoregional recurrence, and 12 (15.4%) and 30 cases (19.1%) of distant metastasis in the TAS and ALND groups, respectively. In the TAS group, 15 patients (19.2%) died and 25 patients (15.9%) died during the follow-up period. All oncologic outcomes based on the breast cancer subtypes are shown in supplementary table 1. In terms of the LRFS, DMFS, and OS, there were no statistical differences in HR-positive breast cancer (LRFS, p = 0.954; DMFS, p = 0.993; and OS, p = 0.617) and HER2-positive breast cancer (LRFS, p = 0.967; DMFS, p = 0.999; and OS, p = 0.423) (Fig. 3,4). However, the OS in the TAS group for TNBC was lower than that in the ALND group, although it was not significant (LRFS, p = 0.411; DMFS, p = 0.697; and OS, p = 0.210) (Fig. 5).

In this study, we compared the 10-year follow-up results of patients with cT1-3N1-2 breast cancer who underwent TAS after NAC with those who underwent conventional ALND after NAC. There were no differences in the oncologic outcomes, including LRFS, DMFS, and OS, between the two groups in all of the patients. In addition, oncological outcomes showed no differences across the molecular subtypes, including HR-positive, HER2-positive, and TNBC.

Initially, the primary objective of NAC in breast cancer was to achieve resectability in inoperable locally advanced or inflammatory breast cancer^23–25. Furthermore, NAC allowed the use of breast-conserving surgery rather than mastectomy and enabled monitoring of the tumor response^26–28. Recently, the goal of NAC in breast cancer has changed to the achievement of pCR, which is a predictive surrogate marker of a better prognosis^29,30. However, to verify the pCR of breast cancer, the exact cancer tissues should be pathologically evaluated.

Because of postoperative morbidities, such as lymphedema and nerve injury, the concept of partial ALND was introduced for patients with node-negative breast cancer by several surgeons^31–33. However, rather than simply resecting part of the ALND, a targeting technique is required for node-positive breast cancer. To address this problem, it is important to mark the primary tumor and positive axillary lymph nodes for tracking during and after NAC. Several methods, including the placement of a clip or radioactive seed and charcoal tattooing, have been developed^8–12. Although many novel techniques have been introduced, long-term oncologic outcomes remain underreported.

Our team reported the 5- and 10-year oncologic outcomes of patients with node-positive breast cancer who received upfront surgery with TAS compared with those that received ALND^22,34. In the serial oncological outcomes, the TAS group consistently indicated non-inferiority compared with the ALND group. Additionally, a similar trend was observed in this study focusing on patients who received prior chemotherapy.

It is important to explore how TAS, a surgical technique that has not yet been standardized, can be beneficial for patients compared with the traditional ALND approach. First, by targeting the exact lesion, accurate information can be obtained to determine the tumor response after NAC in breast cancer. Although it is uncommon to miss metastasis-proven lymph nodes during conventional ALND, because the structure of lymph nodes becomes faint as they are replaced by fatty changes and fibrosis^35–37, there is a possibility of this occurring. Second, the rate of lymphedema is significantly higher in patients who received ALND than in those who received TAS with axillary radiotherapy³⁸. Because it is impossible to be completely cured and the quality of life deteriorates once lymphedema occurs, prevention is the most important consideration for lymphedema^39–41. Third, the operative time can be reduced when TAS is applied, and there are fewer sequelae, including bleeding or paresthesia, because the blood vessels or nerve structures are relatively less exposed.

In this study, the authors compared the TAS group with or without axillary radiotherapy and the ALND group in patients with node-positive breast cancer who received NAC and showed consistent oncologic outcomes across the breast cancer subtypes. Although the difference between the two groups in TNBC was somewhat increased during the 10-year follow-up period, statistical significance was lacking. This indicates that the TAS procedure can be applied to patients with N1-2 breast cancer after NAC. However, if the breast cancer is higher than N3 or has a high tumor burden in the axillary lymph nodes even after NAC, it would be better to proceed with ALND.

To the best of our knowledge, this study represents a pioneering long-term oncologic report of patients with node-positive breast cancer who underwent NAC followed by TAS. Pretreatment with chemotherapy may induce lymphedema in the arms even before surgical intervention, and ALND often fails to sufficiently mitigate this condition. Consequently, TAS has emerged as a viable alternative, particularly for patients who respond positively to NAC. Despite the inherent limitations of a retrospective design and a relatively small cohort, this study underscores the potential of TAS as a standard treatment option within this patient population.

Author Contributions:

Conceptualization, JL, WHK, HJK and HYP; methodology, JL, HYP, and BK; validation, SJL, YSC, IHL; investigation, BK, and JHJ; clinical practice; JL, WHK, HJK, J-YP, NJP, and HYP; resources, BK; data curation, JL, JHJ, and BK; writing – original draft preparation, JL; writing, review, and editing; JL, HYP, and JHJ; visualization, JL; supervision, HYP.

Institutional Review Board Statement:

This study was approved by the Institutional Review Board Committee of the Kyungpook National University Chilgok Hospital, Daegu, Republic of Korea (KNUCH 2015-05-205). In addition, specific inclusion and exclusion criteria were defined according to the approved institutional review board protocol.

Informed Consent Statement:

Informed consent was obtained from all the participants involved in this study.

Data Availability Statement:

The datasets generated and analyzed during the current study are not publicly available. However, they are available from the corresponding author upon reasonable request.

Acknowledgments:

Not applicable

Conflicts of Interest:

The authors declare no conflicts of interest.

Funding:

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (2014R1A5A2009242, 2022R1F1A1072458) and this research was supported by the Bio &Medical Technology Development Program of the National Research Foundation (NRF) funded by the Ministry of Science & ICT (2017M3A9G8083382) and this work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2022R1I1A1A01070224). This research was supported by a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (HR22C1832).

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No competing interests reported.

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10-Year Outcomes of Targeted Axillary Surgery after Neoadjuvant Chemotherapy in Breast Cancer

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