Comparison of Long-term Oncological Outcome of Sentinel Lymph Node Mapping Methods (Dye-Only versus Dye and Radioisotope) in Breast Cancer Patients Following Neoadjuvant Chemotherapy

Jinyoung Byeon; Changjin Lim; Eunhye Kang; Ji-Jung Jung; Hong-Kyu Kim; Han-Byoel Lee; Hyeong-Gon Moon; Wonshik Han

doi:10.4143/crt.2024.1253

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Original Article Breast cancer Comparison of Long-term Oncological Outcome of Sentinel Lymph Node Mapping Methods (Dye-Only versus Dye and Radioisotope) in Breast Cancer Patients Following Neoadjuvant Chemotherapy: Jinyoung Byeon¹, Changjin Lim¹, Eunhye Kang¹, Ji-Jung Jung¹, Hong-Kyu Kim^1,2,3, Han-Byoel Lee^1,2,3, Hyeong-Gon Moon^1,2,3, Wonshik Han^1,2,3; Cancer Research and Treatment : Official Journal of Korean Cancer Association 2026;58(1):175-181.
DOI: https://doi.org/10.4143/crt.2024.1253
Published online: April 15, 2025

¹Department of Surgery, Seoul National University Hospital, Seoul National University College of Medicine, Seoul, Korea

²Cancer Research Institute, Seoul National University College of Medicine, Seoul, Korea

³Biomedical Research Institute, Seoul National University College of Medicine, Seoul, Korea

Correspondence: Wonshik Han, Department of Surgery, Seoul National University Hospital, Cancer Research Institute, Seoul National University, 101 Daehak-ro, Jongno-gu, Seoul 03080, Korea
Tel: 82-2-2072-1958 E-mail: hanw@snu.ac.kr

• Received: December 30, 2024 • Accepted: April 13, 2025

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Abstract

Purpose
Sentinel lymph node biopsy (SLNB) using dye and isotope (DUAL) is recommended over the dye-only (DYE) method after neoadjuvant chemotherapy (NCT) due to potentially lower false-negative rates. However, the long-term outcome of either method is unclear. We aimed to compare the long-term oncological outcomes of DYE versus DUAL SLNB methods in patients who received NCT.
Materials and Methods
In this retrospective cohort study, 893 patients who underwent SLNB following NCT and had pathologically negative lymph nodes were included. After propensity score matching for cT, cN, and pT categories, 280 patients were in the DYE group and 560 in the DUAL group. Indigo carmine was used for dye and Tc-99m antimony trisulfate for isotope mapping.
Results
Median follow-up was 75.6 months in the DYE group and 83.0 months in the DUAL group. Mean (±standard deviation) number of harvested sentinel nodes was 6.7 (±3.9) and 6.7 (±3.3) in the DYE and DUAL groups (p=0.875). Five-year distant metastasis-free survival was 95.2% in DYE group and 93.3% in DUAL group (hazard ratio [HR], 1.45; 95% confidence interval [CI], 0.82 to 2.57; p=0.192). Disease-free survival (HR, 0.97; 95% CI, 0.69 to 1.50; p=0.914) and overall survival (HR, 0.98; 95% CI, 0.56 to 1.69; p=0.954) were not significantly different. Axillary recurrence rate was 1.8% and 2.5% in DYE and DUAL groups (p=0.647).
Conclusion
Long-term oncological outcomes did not significantly differ between DYE and DUAL SLNB methods. The dye-only method can be safely recommended for breast cancer patients who received NCT.
Key words: Breast neoplasms, Sentinel lymph node mapping, Dye-only method, Oncologic outcome

Introduction

In breast cancer, axillary lymph node dissection (ALND) has been replaced by sentinel lymph node biopsy (SLNB) for nodal staging [1] with significantly less morbidity [2-4]. The most clinically feasible methods for sentinel node identification are dye injection or radioisotope tracer mapping methods. In a study, dye mapping only, radioisotope mapping only, and dual-tracer methods had sentinel lymph node (SLN) detection rates of 90%, 95%, and 98%, respectively [5]. Another meta-analysis reported that the use of blue dye alone was associated with the highest false-negative rate (FNR) compared with that of a radioactive tracer alone or a combination of both [6]. Thus, there are concerns about the inferiority of the dye-only technique. However, our previous study showed that dye alone for SLNB was not inferior to dual mapping regarding long-term oncological outcomes in early breast cancer [7].

Currently, SLNB is also performed following neoadjuvant chemotherapy (NCT), although there are some controversies for patients who initially had a clinical node-positive disease [8-11]. In the ACOSOG Z1071 trial, the FNR of SLNB was 12.6%, exceeding the predefined acceptable rate of 10%. However, subgroup analysis showed lower FNR in patients with the use of immunohistochemistry and clipping of biopsy-proven metastatic nodes prior to chemotherapy [12]. As a result of the following trials investigating SLNB in clinical node-positive patients and patients who received NCT, targeted axillary dissection (TAD), removal of at least three sentinel nodes, and dual mapping approaches using both radioisotope and blue dye have been shown to reduce FNR to ≤ 10% [9,11,13].

However, the radioisotope method exposes physicians and patients to radiation and creates an additional burden in the clinical setting with a limited window of time for surgery [14]. The use of radioisotope tracer presents added patient inconvenience, costs, and procedural requirements. Until now, few studies have compared long-term oncologic outcomes between different sentinel lymph node mapping approaches in patients who underwent neoadjuvant treatment. In this study, we aimed to compare the long-term oncological outcome between the two groups who underwent SLNB using either the dye-only method or the combined dye and radiotracer method after NCT.

Materials and Methods

1. Patients

Among patients who underwent breast cancer surgery for primary invasive cancer from January 2005 to December 2013, those who completed NCT before breast cancer surgery and underwent SLNB at the time of surgery were included. Patients with distant metastases or male patients were excluded. Only ypN0 patients, defined as having no residual nodal metastasis after NCT, were included in the analysis. Clinical nodal status (cN) before NCT was assessed using a combination of imaging modalities, including ultrasound, magnetic resonance imaging, and physician’s exam, Needle biopsy was performed for suspicious lymph nodes on imaging. The selection process for the final matched dye-only mapping (DYE) and dye and isotope mapping (DUAL) groups analyzed is depicted in the flow diagram (Fig. 1). Data on patient characteristics for the entire cohort before matching can be found in S1 Table. Data were collected from the Seoul National University Hospital web database using the software CDW SUPREME and manual electronic medical chart reviews for missing data.

2. Definition of endpoint

The main outcome measure was distant metastasis-free survival (DMFS), which was defined as the time from diagnosis to the date of distant metastasis or when censored at the latest date. Secondary endpoints were disease-free survival (DFS), overall survival (OS), and axillary recurrences.

3. Sentinel node mapping procedures

We used a conventional dye injection method for SLNB. After general anesthesia, a 1-mL syringe was used for intradermal injection of indigo carmine dye, 5-15 minutes before the first surgical incision. Typically, the surgeon injects two to four spots around the nipple-areolar complex. After the injection, the surgical team performed a standard SLNB procedure. For the isotope mapping, patients received an injection of Tc-99m antimony trisulfate into the periareolar area at least 1 hour before surgery. A hand-held gamma probe (Neoprobe, Devicor Medical Products, Inc.) was used to identify SLNs with hot uptake. The DUAL method’s dye component was identical to that of the DYE group. If SLNs were not identified using either method, ALND was performed. These cases were excluded from the analysis as they did not meet the study’s inclusion criteria.

4. Statistical analysis

We conducted propensity score matching (PSM) to balance the baseline characteristics between the DYE group and the DUAL group. The selection of matching covariates-clinical T category, clinical N category, and pathologic T category was based on statistically significant differences (p < 0.05) observed between groups prior to matching (S1 Table). Patients were matched using a 1:2 nearest neighbor ratio with a caliper width of 0.3. For survival analysis, a Kaplan-Meier method and a two-sided log-rank test were used. We performed all statistical analyses using SPSS software ver. 25 (IBM Corp.).

Results

1. Demographics and characteristics

After PSM, 280 patients were included in the DYE group and 560 in the DUAL group. The mean (standard deviation [SD]) age was 48.0 (±8.8) years in the DYE group and 48.1 (±10.0) years in the DUAL group (p=0.986). The clinical N category before neoadjuvant therapy (NCT) was cN0 in 14.3% of the DYE group and 19.3% of the DUAL group (p=0.073). No patients in either group underwent preoperative node clipping or TAD. There was no significant difference in patient characteristics between the two groups, including clinical T category, pathologic complete response rate, and tumor subtype (Table 1). The mean (±SD) number of harvested nodes was 6.7 (±3.4) and 6.7 (±3.8) in the DYE and DUAL groups, respectively (p=0.513). When comparing the adjuvant radiotherapy sites between the two groups, there was no significant difference (p=0.295). The proportion of patients receiving adjuvant radiotherapy, including treatment to the breast alone or regional nodes (axilla, supraclavicular lymph node, internal mammary node), was comparable in the groups (Table 2). There was also no difference in surgery method, endocrine therapy, and radiation therapy between the groups.

2. Comparison of oncologic outcome in ypN0 patients between DYE and DUAL groups

The median interquartile range follow-up duration was 75.6 (62.6-100.6) months in the DYE group and 83.0 (66.7-105.1) months in the DUAL group. The 5-year DMFS was 95.2% in the DYE group and 93.3% in the DUAL group, and the 10-year DMFS was 93.7% in the DYE group and 89.6% in the DUAL group (hazard ratio [HR],1.45; 95% confidence interval [CI], 0.82 to 2.57; log-rank p=0.192) (Fig. 2A). The 5-year DFS was 93.1% in the DYE group and 92.7% in the DUAL group, and the 10-year DFS was 73.0% in the DYE group and 75.2% in the DUAL group (HR, 0.97; 95% CI, 0.69 to 1.50; p=0.914) (Fig. 2B). The 5-year OS was 95.9% in the DYE group and 95.1% in the DUAL group, and the 10-year OS was 85.6% in the DYE group and 91.2% in the DUAL group (HR, 0.98; 95% CI, 0.56 to 1.69; log-rank p=0.954) (Fig. 2C). During the follow-up period, the 5-year cumulative incidence of axillary recurrence was 1.8% in the DYE group and 2.5% in the DUAL group (HR, 1.27; 95% CI, 0.45 to 3.58; log-rank p=0.647) (Fig. 2D, S2 Table). Notably, the analysis included only ypN0 patients, defined as those with no residual nodal disease after NCT, and excluded cases with failed SLNB that required ALND.

Discussion

This study demonstrated that there was no significant difference in the long-term oncological outcomes, including DMFS, DFS, and OS, between the dye-only mapping method and the dye-and-isotope dual mapping method in patients who underwent SLNB after NCT. Notably, the cumulative incidence of axillary lymph node recurrence was 1.8% in the DYE group and 2.5% in the DUAL group, highlighting comparable outcomes between the two approaches.

SLNB remains the recommended method for determining axillary lymph node staging in most patients receiving NCT, including those with initial cN0 status and those who convert from cN+ to ycN0 status. However, there is ongoing debate regarding the optimal technique for SLNB in NCT patients, particularly due to concerns about FNR. A recent meta-analysis by Tee et al. [15] demonstrated that the pooled FNR was significantly lower with dual mapping (11%; 95% CI, 6 to 15) compared to single mapping (19%, 95% CI, 11 to 27). They also found that FNR decreased as the number of removed nodes increased: 20% with one node, 12% with two nodes, and 4% with three or more nodes removed [15].

Previous meta-analyses and large prospective trials have consistently reported that single-tracer approaches, particularly dye-only, are associated with lower SLN detection rates (80%-90%) compared with dual-tracer methods (up to 95%-98%), both in primary surgery settings and after neoadjuvant chemotherapy [5,6,11]. For instance, in the SENTINA study, single-tracer mapping yielded an 80.1% detection rate in cN1→ycN0 patients, whereas dual-tracer mapping improved this rate to 87.8% [11]. These findings highlight a potential limitation of dye-only methods, namely, a higher likelihood of identification failure leading to unnecessary ALND and associated morbidity. In our study, we included only patients with successful SLN identification, so we could not directly assess the impact of failed SLNB cases. However, even if these patients had been included, survival outcomes between the groups would likely remain similar. Nevertheless, dye-only mapping may result in a higher ALND rate, which can negatively affect patient quality of life. Given the potential increase in surgical burden and associated morbidity, the implications of using a dye-only approach should be carefully considered in clinical practice.

In our study, the mean number of removed lymph nodes was 6.7, which is higher than typically reported in other studies. This higher node retrieval may have contributed to our favorable outcomes with the dye-only method, as increasing the number of examined nodes has been shown to reduce FNR [15]. Furthermore, our relatively high rate of radiation therapy administration likely provided additional regional control. This is particularly relevant as ongoing trials such as Alliance A11202 [16] and NSABP B-51/RTOG 1304 [17] are investigating the role of regional radiotherapy in managing the axilla after NCT.

In accordance with the de-escalation trend in axilla surgery, an increasing number of studies have aimed to provide the safety of SLNB for patients who received NCT. The primary endpoint of the studies focused on the low and acceptable FNR. These include dual tracer mapping, TAD, finding three or more SLNs, and the MARI approach. For patients who convert from having a clinical node-positive (cN+) to a clinical node-negative (ycN0), FNRs were reported to be higher than primary endpoint [8,9,12,13]. In the SENTINA study, the overall FNR was 14.2% [11]. In the ACOSOGZ1071 trial [13], FNR was 12.6% in cN1 patients with ≥ 2 nodes removed, and in the SN FNAC trial [8], FNR was 13.3%. The conclusions of these studies were the recommendation to use a dual tracer in SLNB to reduce FNR below an acceptable rate. A TAD study ensuring the removal of the clipped node improved the accuracy of SLNB and showed no difference between the use of single versus dual tracers [9]. Our study adds to evidence by suggesting that a dye-only approach may achieve similar long-term oncological outcomes despite concerns about higher FNR in single-tracer methods.

Definitely, we have to wait for the long-term outcome results of these prospective trials and subgroup analyses comparing single versus dual tracers. Meanwhile, our study suggests that dye-only method might not be inferior to the dual-tracer method in terms of long-term oncological outcome and could be safely applied in NCT patients.

Our findings suggest that a modestly higher FNR may not necessarily translate to worse long-term oncological outcomes in carefully selected patients. However, it is important to note that our study focused specifically on comparing dye-only versus dual-tracer methods, and our results should be interpreted within this context. Future prospective studies with larger cohorts and longer follow-up periods will be needed to further validate these findings and potentially identify specific patient subgroups who might benefit most from either approach.

This study has some limitations. First, we analyzed only patients with successful SLN identification and did not track cases of failed SLNB requiring ALND, potentially overestimating the efficacy of the dye-only method. Second, as a retrospective study from a single institution, unmeasured confounders and incomplete data on recurrence or metastasis may limit generalizability. Despite these limitations, the comparable long-term outcomes in patients with successful SLN identification suggest that the dye-only approach can be a cost-effective alternative in settings where radioisotope facilities are limited, provided adequate node sampling is achieved.

In conclusion, our study demonstrated that the dye-only SLN mapping method did not show inferior oncological outcomes such as DMFS, DFS, and OS compared with the dual method using dye and isotope in NCT patients. This finding challenges current guidelines, which favor dual mapping to minimize FNR, and provides evidence supporting a more cost-effective and simplified approach. However, as clinical practices continue to evolve, further studies are needed to explore the long-term impact of SLNB techniques and the feasibility of de-escalating axillary surgery in select patient populations.

Electronic Supplementary Material

Supplementary materials are available at Cancer Research and Treatment website (https://www.e-crt.org).

crt-2024-1253_S1_Table.pdf

crt-2024-1253_S2_Table.pdf

NOTES

Ethical Statement

The study was performed in accordance with the Declaration of Helsinki or comparable ethical standards. This research was approved by the institutional review board (IRB No. 1912-028-1086) of Seoul National University Hospital in South Korea. Requirement for informed consent was waived for all patient because this was a retrospective study.

Author Contributions

Conceived and designed the analysis: Byeon J, Lim C, Han W.

Collected the data: Byeon J, Lim C.

Contributed data or analysis tools: Byeon J, Kang E.

Performed the analysis: Byeon J, Kang E, Jung JJ, Kim HK, Lee HB, Moon HG, Han W.

Wrote the paper: Byeon J, Han W.

Conflicts of Interest

Han-Byoel Lee and Wonshik Han report being a member on the board of directors of and holding stock and ownership interests at DCGen, Co., Ltd., not relevant to this study. Other authors declare no competing interests.

Funding

This research was supported by a grant of Patient-Centered Clinical Research Coordinating Center (PACEN) funded by the Ministry of Health & Welfare, Republic of Korea (grant number: HC19C0110).

Fig. 1.

Patient selection and propensity score matching process for dye-only and dual-tracer methods. DUAL, dye and isotope mapping; NAC, neoadjuvant chemotherapy.

Fig. 2.

Kaplan-Meier curves comparing dye-only (DYE) and dual-tracer (DUAL) methods in terms of distant metastasis-free survival (A), disease-free survival (B), overall survival (C), and axillary recurrence incidence (D) over time. CI, confidence interval; HR, hazard ratio.

Table 1.

Clinicopathologic features of patients after PSM enrolled in the study

Variable	Dye-only method (n=280)	DUAL method (n=560)	p-value
Age (yr)	48.0±8.8	48.1±10.0	0.986
BMI (kg/m²)	23.99±3.30	24.38±3.33	0.114
Clinical T category
1	14 (5.0)	31 (5.5)	0.654
2	213 (76.1)	441 (78.8)
3	38 (13.6)	60 (10.7)
4	15 (5.4)	28 (5.0)
Clinical N category
0	40 (14.3)	108 (19.3)	0.073
1	129 (46.1)	277 (49.5)
2	79 (28.2)	124 (22.1)
3	32 (11.4)	51 (9.1)
Histologic grade
I/II	134 (47.9)	279 (49.8)	0.346
III	126 (45.0)	253 (45.2)
Unknown	20 (7.1)	28 (5.0)
pCR
No	165 (58.9)	330 (59.0)	0.487
Yes	115 (41.1)	230 (40.0)
Pathologic T category
0	115 (41.1)	230 (41.1)	0.185
1	104 (37.1)	237 (42.3)
2	53 (18.9)	85 (15.2)
3	8 (2.9)	8 (1.4)
Harvested LN	6.70±3.96	6.74±3.34	0.875
Tumor subtype
HR+/HER2–	100 (35.7)	185 (33.0)	0.590
HR+/HER2+	58 (20.7)	109 (19.5)
HR–/HER2+	53 (18.9)	103 (18.4)
TNBC	69 (24.6)	163 (29.1)

Values are presented as mean±SD or number (%). BMI, body mass index; DUAL, dye and isotope mapping; HER2, human epidermal growth factor receptor 2; HR, hormone receptor; LN, lymph node; pCR, pathologic complete response; PSM, propensity score matching; SD, standard deviation; TNBC, triple-negative breast cancer.

Table 2.

Comparison of treatment and adjuvant therapies after PSM enrolled in the study

Variable	Dye-only method (n=280)	DUAL method (n=560)	p-value
Treatment characteristics
Type of breast surgery
BCS	204 (72.9)	423 (75.5)	0.400
Mastectomy	76 (27.1)	137 (24.5)
HER2 target therapy
Yes	108 (38.6)	208 (37.1)	0.743
No	172 (61.4)	352 (62.9)
Adjuvant radiotherapy
Breast	91 (32.5)	175 (31.3)	0.295
Breast+Axilla+SCL	101 (36.0)	232 (41.4)
Breast+Axilla+SCL+IMN	76 (27.1)	124 (22.1)
Unknown	12 (4.3)	29 (5.2)
Adjuvant endocrine therapy
Yes	155 (55.4)	321 (52.4)	0.449
No	125 (44.6)	239 (47.6)

Values are presented as number (%). BCS, breast-conserving surgery; DUAL, dye and isotope mapping; HER2, human epidermal growth factor receptor 2; IMN, internal mammary nodes; PSM, propensity score matching; SCL, supraclavicular lymph node.

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10. Hunt KK, Yi M, Mittendorf EA, Guerrero C, Babiera GV, Bedrosian I, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy is accurate and reduces the need for axillary dissection in breast cancer patients. Ann Surg. 2009;250:558–66. Article PubMed
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12. Boughey JC, Ballman KV, Hunt KK, McCall LM, Mittendorf EA, Ahrendt GM, et al. Axillary ultrasound after neoadjuvant chemotherapy and its impact on sentinel lymph node surgery: results from the American College of Surgeons Oncology Group Z1071 Trial (Alliance). J Clin Oncol. 2015;33:3386–93. Article PubMed PMC
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Comparison of Long-term Oncological Outcome of Sentinel Lymph Node Mapping Methods (Dye-Only versus Dye and Radioisotope) in Breast Cancer Patients Following Neoadjuvant Chemotherapy

Cancer Res Treat. 2026;58(1):175-181. Published online April 15, 2025

DOI: https://doi.org/10.4143/crt.2024.1253

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Abstract
Introduction
Materials and Methods
Results
Discussion
Electronic Supplementary Material
NOTES
REFERENCES

Comparison of Long-term Oncological Outcome of Sentinel Lymph Node Mapping Methods (Dye-Only versus Dye and Radioisotope) in Breast Cancer Patients Following Neoadjuvant Chemotherapy

Fig. 1. Patient selection and propensity score matching process for dye-only and dual-tracer methods. DUAL, dye and isotope mapping; NAC, neoadjuvant chemotherapy.

Fig. 2. Kaplan-Meier curves comparing dye-only (DYE) and dual-tracer (DUAL) methods in terms of distant metastasis-free survival (A), disease-free survival (B), overall survival (C), and axillary recurrence incidence (D) over time. CI, confidence interval; HR, hazard ratio.

Fig. 1.

Fig. 2.

Comparison of Long-term Oncological Outcome of Sentinel Lymph Node Mapping Methods (Dye-Only versus Dye and Radioisotope) in Breast Cancer Patients Following Neoadjuvant Chemotherapy

Variable	Dye-only method (n=280)	DUAL method (n=560)	p-value
Age (yr)	48.0±8.8	48.1±10.0	0.986
BMI (kg/m²)	23.99±3.30	24.38±3.33	0.114
Clinical T category
1	14 (5.0)	31 (5.5)	0.654
2	213 (76.1)	441 (78.8)
3	38 (13.6)	60 (10.7)
4	15 (5.4)	28 (5.0)
Clinical N category
0	40 (14.3)	108 (19.3)	0.073
1	129 (46.1)	277 (49.5)
2	79 (28.2)	124 (22.1)
3	32 (11.4)	51 (9.1)
Histologic grade
I/II	134 (47.9)	279 (49.8)	0.346
III	126 (45.0)	253 (45.2)
Unknown	20 (7.1)	28 (5.0)
pCR
No	165 (58.9)	330 (59.0)	0.487
Yes	115 (41.1)	230 (40.0)
Pathologic T category
0	115 (41.1)	230 (41.1)	0.185
1	104 (37.1)	237 (42.3)
2	53 (18.9)	85 (15.2)
3	8 (2.9)	8 (1.4)
Harvested LN	6.70±3.96	6.74±3.34	0.875
Tumor subtype
HR+/HER2–	100 (35.7)	185 (33.0)	0.590
HR+/HER2+	58 (20.7)	109 (19.5)
HR–/HER2+	53 (18.9)	103 (18.4)
TNBC	69 (24.6)	163 (29.1)

Variable	Dye-only method (n=280)	DUAL method (n=560)	p-value
Treatment characteristics
Type of breast surgery
BCS	204 (72.9)	423 (75.5)	0.400
Mastectomy	76 (27.1)	137 (24.5)
HER2 target therapy
Yes	108 (38.6)	208 (37.1)	0.743
No	172 (61.4)	352 (62.9)
Adjuvant radiotherapy
Breast	91 (32.5)	175 (31.3)	0.295
Breast+Axilla+SCL	101 (36.0)	232 (41.4)
Breast+Axilla+SCL+IMN	76 (27.1)	124 (22.1)
Unknown	12 (4.3)	29 (5.2)
Adjuvant endocrine therapy
Yes	155 (55.4)	321 (52.4)	0.449
No	125 (44.6)	239 (47.6)

Table 1. Clinicopathologic features of patients after PSM enrolled in the study

Table 2. Comparison of treatment and adjuvant therapies after PSM enrolled in the study