Abstract
This study aimed to evaluate the locoregional recurrence-free survival (LRFS) associated with breast-conserving surgery (BCS) based on the regressed tumor extent after neoadjuvant chemotherapy (NAC) (neoadjuvant group) versus upfront BCS without NAC (adjuvant group) in nonmetastatic Chinese patients. Two approaches of 1:1 propensity score matching (PSM), pre-NAC and post-NAC baseline matching, were employed. In the pre-NAC baseline matching, clinicopathological features prior to NAC in the neoadjuvant group were matched with corresponding features in the adjuvant group; whereas in the post-NAC baseline matching, the features after NAC in the neoadjuvant group were matched with those in the adjuvant group. Baseline characteristics were well balanced between groups after matching, with a median follow-up duration of 50.8 months. In the pre-NAC baseline matching, a total of 553 case pairs were matched. The 5-year LRFSs did not significantly differ between neoadjuvant and adjuvant groups (94.37% vs 93.85%, P > 0.05), nor did the 8-year LRFSs (91.80% vs 92.08%, P > 0.05). In the post-NAC baseline matching, 645 case pairs were included. Again, no statistically significant differences were observed in the 5-year (94.78% vs. 92.44%, P > 0.05) and 8-year LRFS (91.26% vs. 89.67%, P > 0.05) between the two groups. Subgroup analyses stratified by RECIST response and tumor shrinkage extent likewise demonstrated no significant difference in both approaches. These findings indicate that, under contemporary treatment regimens and surgical standards, post-NAC BCS based on the regressed tumor extent did not increase the risk of locoregional recurrence in Chinese patients.
Keywords: Breast cancer, Breast-conserving surgery, Neoadjuvant chemotherapy
Highlights
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Two approaches of propensity score matching were applied using pre- and post-NAC baseline characteristics respectively.
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Post-NAC BCS based on regressed tumor extent shows comparable local control to upfront BCS in nonmetastatic Chinese patients.
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Subgroup analyses stratified by REClST response or tumor shrinkage did not reveal significant difference.
1. Introduction
Since the advent of neoadjuvant chemotherapy (NAC) in breast cancer management, its principal aims have been to (1) downstage large tumors (Stage III or > T2 tumors) to increase the eligibility of breast-conserving surgery (BCS); (2) assess tumor response to chemotherapy in order to guide subsequent treatment [[1], [2], [3]]. According to the St. Gallen consensus, the majority of experts advocated for surgical resection based on the regressed tumor extent after NAC, which would increase the breast conservation rate [4]. However, heterogeneous tumor regression underscores the possibility that residual tumor cells may persist in the original tumor range. A series of studies had investigated the pathological patterns of tumor regression and generally stratified them into concentric shrinkage (CS) and non-concentric shrinkage (NCS) [[5], [6], [7], [8]]. Concerns had thus been raised regarding the residuals increasing the risk of locoregional recurrence (LRR), especially in patients with NCS pattern [9]. A pivotal EBCTCG meta-analysis revealed that the 15-year LRR was 3.2% higher in the NAC group compared to the adjuvant chemotherapy (AC) group [10], which appeared to support the assumption.
It is important to note, however, that the patient cohorts included in previous studies were treated with outdated therapeutic regimens. It remains unclear whether the same surgical approach to BCS would still be associated with an increased risk of LRR in patients receiving contemporary treatment. Meanwhile, according to the guidelines of the Chinese Society of Breast Surgery (CSBrS), a consensus has yet to be reached regarding the optimal extent of surgery following NAC [1]. This is primarily attributed to: (1) concerns about the limited accuracy in assessing the degree of post-NAC tumor shrinkage; and (2) the paucity of clinical data on LRR among Chinese patients, who present distinct characteristics such as smaller breast volume, a higher proportion of younger individuals and denser breast tissue compared to their counterparts in Western populations. We hereby conducted this study to investigate the LRR of post-NAC based on the regressed tumor extent in order to provide clinical evidence to its safety concern in Chinese patients.
2. Method
2.1. Study design
This study was a single-centered retrospective cohort analysis. A total of 8563 patients who underwent surgical treatment for breast cancer at the Sun Yat-sen Memorial Hospital, Sun Yat-sen University, between January 1st, 2000, and August 31st, 2023, were primarily evaluated. The neoadjuvant group was defined as patients who achieved either complete response (CR) or partial response (PR) according to the Response Evaluation Criteria in Solid Tumors (RECIST) following NAC [11] and subsequently underwent BCS. The adjuvant group was defined as those who underwent direct BCS without NAC.
2.2. Inclusion and exclusion criteria
The eligibility criteria for inclusion required a confirmed diagnosis of unilateral breast cancer, with clinical staging from stage 0 to stage III, and the absence of distant metastasis at the time of diagnosis. Patients were excluded from the study if they presented with bilateral breast cancer, accessory breast carcinoma, occult breast cancer, distant metastases prior to surgical intervention, phyllode tumors, or malignant neoplasms of mesenchymal origin. Additionally, individuals with incomplete demographic, clinical or follow-up information were also excluded for data integrity and analytical rigor.
Given its retrospective nature, real-world data from our medical records were collected for the purpose of integrity, including all the treatments received. Our physicians were instructed to follow the updated National Comprehensive Cancer Network (NCCN) and Chinese Society of Clinical Oncology Breast Cancer (CSCO) guidelines when selecting candidates for NAC and planning for adjuvant strategies [[2], [12]]. It was noteworthy that trastuzumab was not widely incorporated into HER2 treatment protocols in our center prior to 2009.
2.3. Data collection and definition
Data including patients' demographic and clinical characteristics were collected. A standard follow-up protocol was abided on an annual basis from the date of operation until September 20, 2024. Other outpatient, inpatient and telephone interviews were supplemented if necessary.
In this study, estrogen receptor positivity was defined as its expression of 1-3+ prior to 2007, or as >10% positively stained tumor cells according to immunohistochemistry (IHC) after 2007; similarly, progesterone receptor (PR) positivity after 2007 was as >1%, in accordance with evolving international guidelines. The human epidermal growth factor receptor 2 (HER2) status was determined using the HercepTest assay. Tumors were classified as HER2-positive if they exhibited a score of 3+ by IHC, or a score of 2+ with confirmed HER2 gene amplification as determined by fluorescence in situ hybridization (FISH). Tumors with a HercepTest score of 0-1+, or a score of 2+ without gene amplification, were classified as HER2-negative [13]. Both clinical and pathological staging were determined in accordance with the 8th edition of the American Joint Committee on Cancer (AJCC) TNM classification for breast cancer [14]. Initial cT/cN represented the clinical T/N stage before NAC in neoadjuvant group and preoperative clinical T/N stage in the adjuvant group. ycT/ypN meant the post-NAC clinical T/pathological N stage in the neoadjuvant group, and preoperative clinical T/pathological N stage in the adjuvant group likewise. Tx was defined as those who had undergone vacuum-assisted breast biopsy or other excisional procedures prior to surgery in the BCS group, or the primary tumor could not be accurately assessed. Nx was defined as ambiguous or missing clinical and radiological axillary lymph node assessments.
In terms of the BCS, our institution followed the NCCN and Chinese Society of Breast Surgery (CSBrS) guidelines [1,2]. Intraoperative frozen and postoperative paraffin section were used to evaluate margin status of BCS [13,15]. Pathologically negative margins confirmed by paraffin section were obtained eventually in all surgical patients enrolled. The recurrence was determined based on evidence from routine diagnostic imaging modalities or biopsy confirmation. Locoregional recurrence was defined as the ipsilateral recurrence of breast malignancy in the breast parenchyma, skin, surgical scar or regional lymph nodes after BCS. Mortality was defined as decease confirmed by an official death certificate or as reported by the patient's family.
2.4. Statistical design and analysis
In this study, we implemented two propensity score matching (PSM) approaches to enhance the robustness of our comparative analysis (Fig. 1).
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(1)
Pre-NAC Baseline Matching: We matched the initial clinicopathological features of patients who underwent NAC followed by BCS (neoadjuvant) prior to receiving NAC, with the corresponding preoperative clinicopathological features of patients who underwent BCS without NAC (adjuvant). The aim of this pre-NAC approach was to investigate whether BCS patients with similar tumor burdens before treatment had decreased locoregional recurrence-free survival (LRFS) in the neoadjuvant group compared to the adjuvant group.
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(2)
Post-NAC Baseline Matching: We matched the clinicopathological features of patients in the neoadjuvant group after completion of NAC with the corresponding preoperative clinicopathological features of those in the adjuvant group. The aim of the post-NAC approach was to compare patients who achieved downstaging after NAC and subsequently underwent BCS, regardless of their initial tumor burden, with patients in the adjuvant group at the same pathological stage, to determine whether LRFS was decreased in the neoadjuvant group.
Fig. 1.
Illustration of two baseline matching strategies.
Propensity scores were computed using a multivariate logistic regression model to incorporate relevant covariates between the groups. A 1:1 nearest-neighbor propensity score matching (PSM) algorithm with a caliper of 0.01 was employed to ensure precise covariate balance.
Survival outcomes were evaluated using the Kaplan–Meier (K-M) method, with intergroup comparisons performed via log-rank test. K-M survival curves were graphically rendered using GraphPad Prism software. The median duration of follow-up was estimated using the reverse K-M technique. Hazard ratios (HRs) and corresponding 95% confidence intervals (CIs) were derived from Cox proportional hazards regression models to quantify the strength of associations. All statistical analyses and graphs were conducted using R software (version 4.4.1) in conjunction with necessary analytical packages within the R-Studio environment. The tables were transfigured by WPS 2025.
3. Results
3.1. Pre-NAC baseline matching
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Baseline Characteristics Before and After Matching
Prior to PSM, a total of 5060 breast cancer patients were included in this study, comprising 4283 individuals in the adjuvant group and 777 patients in the neoadjuvant group. A notable imbalance in sample size was observed between the two groups, as well as in the analyses of most subgroups (Supplemental Table 2.1). To investigate whether patients with similar tumor burdens at baseline may have decreased LRFS when they received NAC before BCS (neoadjuvant group) versus those in the adjuvant group, we performed PSM for a total of 553 case pairs (Fig. 2). The distribution of propensity scores was well balanced between the two groups (Supplemental Fig. 2.3), with standardized mean differences (SMDs) for all covariates below 0.1 (Supplemental Fig. 2.4). The baseline characteristics of the two groups were generally at equilibrium and significant imbalances seen in the original datasets were since eliminated.
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Locoregional Recurrence-Free Survival, Univariate and Multivariate Analyses
Fig. 2.
Flow diagram of participant selection before and after Pre-NAC baseline matching.
The median follow-up time for the neoadjuvant group was 50.8 months, while that for the adjuvant group was 44.9 months. Owing to the relatively small number of follow-up extension beyond 10 years, the survival analysis was confined to outcomes observed within 8 years of enrollment, thereby ensuring the interpretative reliability of the survival estimates.
The rate of loss to follow-up were 3.98% (22 of 553 patients) in the neoadjuvant group, and 4.52% (25 of 553 patients) in the adjuvant group. The cumulative incidence of LRR at 5 years was 4.71% (25 of 531 patients) in the neoadjuvant group and 4.17% (22 of 528 patients) in the adjuvant group, rising modestly to 5.08% (27 of 531 patients) and 4.73% (25 of 528 patients) respectively at 8 years. Despite numerically lower recurrence rates in the neoadjuvant group, the difference in LRFS between the two groups was not statistically significant. The LRFS at 8 years was 92.08% in the neoadjuvant group compared to 91.80% in the adjuvant group (HR = 1.04; 95% CI: 0.62–1.76; P = 0.875), indicating comparable long-term local control between treatment strategies (Fig. 3). Both univariate and multivariate Cox proportional hazards regression analyses were performed on the PSM cohorts. Given that tumor T-stage is a clinically crucial factor for LRR, it was included in the multivariate analyses. The results demonstrated that the neoadjuvant group did not show a statistically significant difference in LRFS compared to the adjuvant group (Supplemental Table 2.2).
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Subgroup Analyses of Locoregional Recurrence-Free Survival
Fig. 3.
Kaplan–Meier (K-M) analysis of LRFS after Pre-NAC baseline matching.
To further examine the consistency of findings across clinically meaningful subpopulations, an exploratory subgroup analysis was conducted within the PSM cohort (Supplemental Figure 2.5). The LRFSs between the neoadjuvant and the adjuvant group remained statistically insignificant across all examined subgroups. Among patients who achieved PR, the LRFS did not differ significantly from that of the adjuvant group, with a HR of 1.12 (95% CI: 0.66–1.90; P = 0.669). Meanwhile, only one LRR event was observed in the subgroup of patients who achieved CR and yet no difference in HR had been revealed (Supplemental Fig. 2.6). To assess the impact of absolute tumor diameter reduction after NAC on LRFS, patients in the neoadjuvant group were stratified based on whether the post-chemotherapy tumor size reduction exceeded 2 cm. No statistically significant difference in HR was observed in either subgroup analysis (Supplemental Fig. 2.7).
3.2. Post-NAC baseline matching
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4
Baseline Characteristics Before and After Matching
In this section, A total of 6720 participants were included (Fig. 4). Among them, 781 patients (11.6%) received NAC followed by BCS (neoadjuvant group), while 5939 patients (88.4%) underwent upfront BCS (adjuvant group). Substantial imbalances in baseline clinical and pathological features were still observed between the two groups (Supplemental Table 3.1). Again, after PSM, 645 pairs of patients were selected and no significant difference was observed in regard to propensity score (Supplemental Fig. 3.3), SMDs (Supplemental Fig. 3.4) and other features alike.
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Locoregional Recurrence-Free Survival, Univariate and Multivariate Analyses
Fig. 4.
Flow diagram of participant selection before and after Post-NAC baseline matching.
The median follow-up duration of the neoadjuvant group was 51.1 months, while that in the adjuvant group was slightly longer at 44.8 months. After PSM, loss to follow-up was infrequent and comparable between the two groups, with rates of 3.72% (24 of 645 patients) in the neoadjuvant group and 4.50% (29 of 645 patients) in the adjuvant group. The cumulative 5-year LRR was 5.63% in the neoadjuvant group (35 events) versus 3.57% in the adjuvant group (22 events). By 8 years, the LRRs were 6.28% and 4.55%, respectively. Although numerically higher recurrence was observed in the neoadjuvant group, the difference was not statistically significant. The estimated 8-year LRFS was 89.67% in the neoadjuvant group compared to 91.26% in the adjuvant group (HR = 1.40, 95% CI: 0.88–2.23; P = 0.160) (Fig. 5), suggesting that BCS after NAC did not confer a statistically significant decrease in the LRFS. The univariate and multivariate Cox proportional hazards analyses revealed no statistically significant difference between the two groups (Supplemental Table 3.2).
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Subgroup Analyses of Locoregional Recurrence-Free Survival
Fig. 5.
Kaplan–Meier (K-M) analysis of LRFS after Post-NAC baseline matching.
Subgroup analysis revealed no significant heterogeneity across a wide range of clinicopathological subgroups. Among all predefined subgroups, no statistical difference in LRFS was observed between the two surgical strategies (Supplemental Fig. 3.5). Among patients who achieved CR to NAC, two LRR events were observed during the follow-up period. In the PR subgroup,patients in the neoadjuvant group exhibited a numerically higher but statistically non-significant risk compared to their adjuvant counterparts; a similar non-significant pattern was seen in the CR subgroup (Supplemental Fig. 3.6). No significant difference of LRFS in either the tumor size reduction of >2 cm or ≤2 cm subgroup was observed (Supplemental Fig. 3.7).
4. Discussion
This study examined the ongoing debate regarding the safety of BCS based on regressed tumor region after NAC in a Chinese population, employing two distinct propensity score matching strategies to ensure robust comparison. After using pre-NAC and post-NAC baselines matching respectively, the 8-year LRFSs between the neoadjuvant and the adjuvant group demonstrated no statistically significant difference. The 5-year LRFSs in the neoadjuvant group (93.85% and 92.44%) closely mirrored the outcomes of post-neoadjuvant treatment in the MSKCC study (93.7%) [16] and a recent retrospective study conducted in South Korea (92.3%) [17]. Specifically, the absolute differences in the 8-year LRRs were 0.35% (5.08% vs. 4.73%) and 1.73% (6.28% vs. 4.55%) in the two matched groups, substantially lower than that of the 10-year LRR reported in the EBCTCG meta-analysis (3.2%) [10].
The primary reason why our results did not replicate the differences in LRR reported by the EBCTCG study may lie in the patient cohorts. While the EBCTCG meta-analysis included data from 1983 to 2002, our patients represent a more contemporary population treated between 2000 and 2023. This temporal shift encapsulates several significant advancements: (1) the adoption of more refined and subtype-specific regimens, including a broader array of therapeutic agents with targeted therapies and standard post-BCS radiotherapy [[18], [19], [20]]; (2) the integration of advanced imaging modalities and localization techniques, such as intraoperative mammography for margin assessment [21], the use of clips [22,23], and higher-resolution MRI with DCE [24], all of which have enhanced surgical precision; (3) improved methods for evaluating NAC response, exemplified by tools like the Lucerne Toolbox [25], which have further optimized surgical decision-making.
As previous studies have discussed that post-NAC tumors can exhibit two distinct regression patterns (CS and NCS), a retrospective synthesis of the literature suggests that tumors with a high initial tumor burden and those of the luminal subtype are more frequently associated with NCS regression [26,27]. These alternative regression patterns likely reflect different risks of recurrence across patient subgroups. However, our study did not reveal any significant difference in overall recurrence risk or in subgroup analyses, regardless of the matching methods.
Over the course of our follow-up period, only one and two LRR events were observed in the CR subgroup, respectively. Although this observation is limited by the smaller sample size of CR patients compared to those with PR, the low event rate suggests that, in a larger cohort, the true LRR in the CR subgroup may be substantially lower than that in the PR group. Notably, the high rates of pCR following NAC, exceeding 60% in patients with HER2-overexpressing and TNBC [[28], [29], [30]], have sparked growing interest in the potential to omit surgery in patients achieving CR after NAC. This emerging paradigm introduces a novel direction in the surgical management of breast cancer. A recent trial focused on patients with a vacuum-assisted core biopsy (VACB)-confirmed pCR following neoadjuvant systemic therapy (NST) were managed without surgery [31]. Remarkably, over a median follow-up of 26.4 months, no cases of local or distant recurrence were reported. These findings underscore the possibility that, in carefully selected patients, omission of surgery may not compromise oncologic safety, even in the presence of residual mosaic tissue following NAC.
Several limitations of our study should be acknowledged. First, it remains challenging to verify that all operating surgeons uniformly adhered to resection strategies strictly guided by the post-NAC regressed tumor, despite of such consensus in our center. Second, due to the retrospective nature of this study, we were unable to conduct a rigorous comparison between “BCS after NAC based on the post-NAC tumor range” versus “BCS after NAC based on the original tumor size”. Our findings yet provided supportive evidence that tailoring the resection to the regressed tumor bed following NAC appears to have little influence on recurrence. Third, adjuvant radiotherapy potentially impacted the local recurrence risk. Despite our physicians were instructed to follow the updated guidelines in practice, the data of radiotherapy were unavailable. Fourth, we did not perform subgroup analyses based on the different shrinkage patterns.
5. Conclusion
In this study, we assessed the LRRs in BCS after NAC in modern Chinese breast cancer patients by employing two analytical strategies of propensity score matching based on pre- and post-NAC baseline characteristics. The results indicated that resection based on the post-NAC regressed tumor extent in BCS does not increase local recurrence. This approach is consistent with the recommendations of the St. Gallen Consensus. Although the Chinese population may present with unique clinicopathological characteristics, our findings support the validity and effectiveness of this surgical strategy in Chinese patients.
CRediT authorship contribution statement
Dongbo Zhang: Writing – original draft, Formal analysis, Data curation. Qianzhu Feng: Writing – original draft, Formal analysis, Data curation. Min Peng: Writing – review & editing, Data curation. Liling Zhu: Writing – review & editing, Funding acquisition. Kai Chen: Supervision, Project administration, Funding acquisition. Shunrong Li: Supervision, Project administration.
Compliance and ethics
The author(s) declare that they have no conflict of interest.
Declaration of interest statement
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This study was sponsored by grants from The Natural Science Foundation of China (#82303552 Recipient: Liling Zhu), Guangdong Provincial Clinical Research Center for Breast Diseases(#2023B110005 Recipient: Erwei Song), Guangdong Science and Technology Department (#2020B1212060018 Recipient: Erwei Song,#2024B1212030002 Recipient: Yan Nie), Guangdong Provincial Development and Reform Commission (#4250022021 Recipient: Erwei Song) and Shanwei Science Technology Commission (#2023A012 Recipient: Kai Chen). The patient cohort was obtained from the Clinical Research and Follow-up Center of Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, GuangZhou, China. Ethical approval for this study was obtained from the Clinical Research Ethics Committee of Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangdong, PRC (Approval No. SYSKY-2025-246-01). Informed consent was waived given the retrospective nature of the study.
Abbreviations
- NAC
neoadjuvant chemotherapy
- AC
adjuvant chemotherapy
- BCS
breast-conserving surgery
- LRR
locoregional recurrence
- LRFS
locoregional recurrence-free survival
- CT
computed tomography
- MRI
magnetic resonance imaging
- PET-CT
positron emission tomography-computed tomography
- PSM
propensity score matching
- CR
complete response
- PR (response)
partial response
- RECIST
response evaluation criteria in solid tumors
- HR
hazard ratio
- CI
confidential interval
- ER
estrogen receptor
- PR (receptor)
progesterone receptor
- HER2
human epidermal growth factor receptor 2
- TNBC
triple negative breast cancer
- CS
concentric shrinkage
- NCS
non-concentric shrinkage
- pCR
pathological complete response
- NCCN
National Comprehensive Cancer Network
- CSCO
Chinese Society of Clinical Oncology Breast Cancer
- CSBrS
Chinese Society of Breast Surgery
- AJCC
American Joint Committee on Cancer
- FISH
fluorescence in situ hybridization
- IHC
immunohistochemistry
- VACB
vacuum-assisted core biopsy
- NST
neoadjuvant systemic therapy
Footnotes
Supplementary data to this article can be found online at https://doi.org/10.1016/j.breast.2026.104775.
Contributor Information
Kai Chen, Email: chenkai23@mail.sysu.edu.cn.
Shunrong Li, Email: lishr@mail.sysu.edu.cn.
Appendix A. Supplementary data
The following is the Supplementary data to this article.
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