Omission of intraoperative frozen section in sentinel lymph node biopsy for early breast cancer: impact on survival outcomes

Introduction

Sentinel lymph node biopsy (SLNB) has become a cornerstone in staging and managing early-stage breast cancer patients with clinically negative nodes, allowing effective disease assessment while avoiding the morbidities of full axillary lymph node dissection (ALND) (1,2). One of the main morbidities of axillary surgery is seroma formation, which remains an unresolved issue despite technological advances and adjunctive measures. This ongoing problem reinforces the rationale for axillary surgery de-escalation strategies, including SLNB and omission of ALND in selected patients, as a more effective means of reducing seroma-related morbidity than technical modifications alone (3-5). The landmark American College of Surgeons Oncology Group Z0011 trial (ACOSOG Z0011) demonstrated in 2017 that patients with one or two positive sentinel lymph nodes (SLNs) did not benefit from ALND in terms of overall or disease-free survival (DFS) (6). Recommendations from the American Society of Clinical Oncology (ASCO) and the National Comprehensive Cancer Network (NCCN) also support omission of completion ALND in patients meeting Z0011 criteria. In this setting, intraoperative evaluation of SLNs is unlikely to alter immediate surgical management and, therefore, is not routinely recommended when the results would not influence intraoperative decision-making (7,8). SLN evaluation is conducted via two main histopathologic methods: intraoperative frozen section (FS) and postoperative permanent section (PS). Traditionally, FS allowed surgeons to perform immediate ALND if SLNs were found to be positive, thereby avoiding second surgeries (9-12). However, following Z0011, the clinical utility of FS has been increasingly questioned. As Godazande et al and Bishop et al. observed, FS usage has declined, especially when metastasis to more than two SLNs is uncommon (12,13). Recent analyses have cast further doubt on FS utility by emphasizing its lower sensitivity and the potential for false negatives (14,15). Recent studies, including those by Wanis et al. and Jung et al., have reported that omitting FS in patients undergoing breast conservative surgery (BCS) did not increase reoperation rates or worsen oncologic outcomes, aligning with updated guidelines recommending more conservative axillary management (16,17). Multiple follow-up studies have shown that there were no differences in DFS and overall survival (OS) between those who underwent SLNB alone and those who received SLNB and ALND (6,18,19). However, limited literature has assessed long-term survival based on the method of SLNB pathological analysis.

At King Chulalongkorn Memorial Hospital, we previously conducted two retrospective studies evaluating the utility of intraoperative FS in early-stage breast cancer patients undergoing breast-conserving surgery (BCS) (20,21). These studies demonstrated that omitting FS did not significantly affect reoperation rates or short-term outcomes and that most patients with SLN metastases did not require further axillary intervention in accordance with ACOSOG Z0011 criteria. In addition, omission of intraoperative FS may offer practical advantages, including reduced operative time, lower healthcare costs, and improved operating room workflow efficiency. While our earlier work focused on immediate clinical endpoints, such as the need for second surgeries, long-term oncologic outcomes including DFS and OS have not been previously reported in this patient population. Therefore, this study serves as a 5-year follow-up of the same cohort of early-stage breast cancer patients who underwent SLNB with or without FS as part of BCS. The aim is to compare DFS and OS between the FS and PS groups and to determine whether omitting intraoperative FS impacts long-term oncologic safety in this surgical context. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2026-0234/rc).

Methods

This retrospective study explored the 5-year survival outcomes of patients with early-stage breast cancer after treatment with different SLNB techniques. The primary focus was to compare the DFS between the FS and PS groups. OS, recurrence at the local and regional levels, and distant metastases were also reported as secondary outcomes. We included all patients who underwent the SLNB procedure at King Chulalongkorn Memorial Hospital from April 2016 to April 2021, with follow-up ending on April 15, 2025. The inclusion criteria were patients with early-stage breast cancer (T1 or T2) with clinically node-negative status who had undergone BCS and SLNB. Postoperative radiotherapy was recommended for all eligible patients in accordance with institutional protocols. However, not all patients received radiotherapy due to individual preferences, including concerns regarding potential side effects or personal beliefs. Patients who had received neoadjuvant chemotherapy and those with noninvasive breast cancer were excluded. A total of 453 SLNB cases were included, of which 239 underwent SLNB using PS alone and 214 underwent the FS technique (Figure 1).

Figure 1 Patient selection flowchart. BCT, breast-conserving therapy; FS, frozen section; PS, permanent section; SLNB, sentinel lymph node biopsy.

Follow-up data were obtained through electronic medical record (EMR) review, including documentation from outpatient clinic visits, imaging studies, and pathology reports within our institution. Outcomes of interest included local recurrence, regional recurrence, distant metastasis, and survival. Events were identified based on clinical, radiological, or pathological confirmation recorded in the EMR. Patients without documented events were considered event-free at the time of last follow-up. Patients who were lost to follow-up were censored at the date of their last recorded clinical visit. Time-to-event outcomes were analyzed using standard survival analysis methods with right censoring. Missing data for baseline clinicopathological variables were minimal, and complete-case analysis was performed. No imputation methods were applied. Data on age, operation type, final pathological diagnosis, tumor staging classification, Nottingham histologic grading, lymphovascular invasion (LVI), human epidermal growth factor receptor 2 (HER-2) and hormonal receptor status and adjuvant treatment were extracted from medical records. Comparison of clinicopathological characteristics between patients with FS and those with PS was also performed. Clinical nodal status was evaluated through physical examination, whereas radiological nodal status was assessed via breast ultrasonography and mammography. SLNB was performed using isosulfan blue dye as a single-agent mapping tracer, which is the standard practice at the King Chulalongkorn Memorial Hospital and throughout Thailand. All pathological diagnoses were based on the serial examination of SLNs using hematoxylin and eosin immunohistochemical staining. Patients were not randomly assigned to the FS or PS group. The decision to perform intraoperative FS was based on routine clinical practice and surgeon preference.

The study protocol was granted a waiver of informed consent owing to the retrospective design, minimal risk to participants, and the use of de-identified data. All data were handled in compliance with institutional data protection policies, and patient confidentiality was strictly preserved, with all identifiers removed prior to analysis. This study was conducted in accordance with the principle of the Declaration of Helsinki and its subsequent amendments. The study was conducted at King Chulalongkorn Memorial Hospital, and the study protocol was reviewed and approved by the Institutional Review Board of the Faculty of Medicine, Chulalongkorn University (COA No. 0985/2025).

Statistical analysis

Microsoft Excel 2019 was used to collect the data extracted from medical records. IBM SPSS Statistics version 26.0 (IBM Corp., Armonk, NY, USA) was utilized for conducting statistical analyses. Categorical data was reported as frequencies and percentages. Pearson chi-square and Fisher exact tests were used to analyze the categorical variables. DFS analysis was defined as the time from SLNB procedure to any event, including local breast cancer recurrences, axillary recurrences, distant metastases, and deaths from all causes. OS analysis was defined as the time from SLNB procedure to deaths from any cause. Local breast cancer recurrence was defined as tumor recurrence in the breast, while regional recurrence referred to ipsilateral axillary recurrences. We employed the Kaplan-Meier method to estimate survival curves. The log-rank test was used to compare FS and PS survival. For the 5-year DFS, the margin was established from the SLNB procedure to the time of event of interest was recorded. Time-to-event outcomes were analyzed using the Kaplan-Meier method and compared with the log-rank test. Cox proportional hazards regression was used to explore factors associated with DFS. The FS group was defined as the reference category. Covariates entered into the multivariable model were selected based on clinical relevance and baseline imbalance between groups, including surgical group (FS vs. PS), LVI and HER-2 status. Categorical variables were entered using indicator coding, with reference categories specified in the model output. Covariates were selected based on both clinical relevance and observed baseline imbalance between groups, including surgical group, LVI, and HER-2 status. Other known prognostic factors were not included in the final multivariable model because the low number of events would have produced unstable estimates. Because this was a retrospective study with a limited number of events, the multivariable model was intended as an exploratory analysis. Formal proportional hazards diagnostics and extensive model optimization were limited by the small number of events. Categorical outcomes of crude event frequencies (e.g., number of recurrence events) were compared using chi-square or Fisher’s exact test (Table 1).

Results

A total of 453 SLNB cases that satisfied the inclusion criteria were included in this study. Two hundred and fourteen operations utilized intraoperative FS, while the remaining 239 operations underwent PS alone. The median [interquartile range (IQR)] follow-up time was 5.3 (4.0–6.2) years in the FS group and 6.3 (5.1–6.5) years in the PS group. Patient age ranged from 26 to 89 years with a mean and median of 56.0 and 55.0 years, respectively. Comparison of clinicopathological features between patients in FS group and those in PS group are demonstrated in Table 2. Seven types of histopathological diagnoses were found in this study: invasive ductal carcinoma (IDC), invasive lobular carcinoma (ILC), ductal carcinoma in situ with micrometastasis (DCISM), mucinous carcinoma, papillary carcinoma, tubular carcinoma and mixed invasive breast carcinoma. IDC accounts for the majority of the histopathological diagnosis, accounting for 373 patients (82.3%). Presence of lymphovascular involvement was found in 93 (20.5%) patients. HER-2 immunohistochemistry status was reported as unknown in 36 cases, due to equivocal HER-2 status and lack of additional fluorescence in situ hybridization (FISH) test. The lack of additional FISH analysis was primarily attributable to patient financial constraints, as the cost of the test was not reimbursable in our healthcare system. Notably, unknown HER-2 status was not evenly distributed between groups. This imbalance may have introduced misclassification bias. Statistically significant differences of LVI status and HER-2 status were found between the FS and PS groups. No significant differences were identified between the FS and PS groups with respect to receipt of adjuvant chemotherapy, radiotherapy, targeted therapy, or in surgical margin status, indicating that the adjuvant treatment strategies and surgical quality outcomes were well-balanced across both cohorts. With respect to surgical margins, a total of 41 patients (9.1%) had positive margins at final pathology, comprising 18 patients (8.4%) in the FS group and 23 patients (9.6%) in the PS group (P=0.65). Re-excision was performed in 6 patients in the FS group and 11 patients in the PS group. The majority of these cases were classified as focally involved margins. In such instances, patients were counseled regarding the risks and benefits of re-excision; however, most declined reoperation. Given that margin involvement was limited to focal disease, and that no statistically significant differences in margin positivity were observed between the FS and PS cohorts, these findings are unlikely to have affected the oncologic outcomes in either group.

Overall, FS sensitivity and specificity for SLN metastasis were 95% and 100%, respectively. Regarding axillary management, four patients in the FS group underwent immediate ALND based on intraoperative findings, and one patient required delayed ALND due to a false-negative FS result. As for PS group, no patient in the PS-only cohort required delayed ALND, and no axillary reoperations were performed. The median number of retrieved SLNs was 2 (IQR, 1–3) in the FS group and 3 (IQR, 2–5) in the PS group. (20,21).

Kaplan-Meier analysis demonstrated a 5-year DFS of 93.5% in the FS group and 95.8% in the PS group. The difference was statistically significant in favor of the PS group [log-rank P=0.008; hazard ratio (HR), 0.34; 95% confidence interval (CI): 0.15–0.79; P=0.01; Figure 2A]. FS was used as the reference category in the Cox model. Subgroups analyses stratified by LVI and HER-2 status showed associations with disease recurrence (adjusted HR, 0.38; 95% CI: 0.17–0.89; P=0.03 and adjusted HR, 0.41; 95% CI: 0.17–0.98; P=0.045, respectively). In multivariable Cox proportional hazards regression, PS remained associated with favorable DFS compared with FS. However, given the limited number of events, this adjusted analysis should be interpreted as exploratory. Overall, DFS events occurred in 14 patients (6.5%) in the FS group and 10 patients (4.2%) in the PS group (P=0.26). OS was similar between the two groups. The 5-year OS did not differ significantly, with no survival disadvantage observed for the PS group compared to the FS group (log-rank P=0.22; HR, 0.40; 95% CI: 0.09–1.83; P=0.24; Figure 2B). A total of seven deaths were recorded: four patients (1.9%) in the FS group and three patients (1.3%) in the PS group, as summarized in Table 1. As for breast cancer-specific survival (BCSS), among the seven deaths observed, only one was attributed to breast cancer, while the remaining six were due to non-cancer-related causes. This finding underscores the excellent BCSS in both cohorts. Note that the P values in Table 1 reflect crude event-count comparisons and the P values reported in the text reflect time-to-event (log-rank) analyses, which account for differences in follow-up time and censoring.

Figure 2 Kaplan-Meier curve of DFS (A), OS (B), local recurrences (C), regional recurrences (D), and distant metastases (E). DFS, disease-free survival; FS, frozen section; OS, overall survival; PS, permanent section.

Local recurrence occurred in 2 patients (0.9%) in the FS group and 3 patients (1.3%) in the PS group (P=0.74). Regional axillary recurrence was observed in 2 patients (0.9%) in the FS group, with no events in the PS group. Distant metastases occurred in 8 patients (3.7%) in the FS group and 6 patients (2.5%) in the PS group (P=0.45). Two patients in each group experienced both local recurrence and distant metastasis. Kaplan-Meier analysis revealed no significant difference in local recurrence (log-rank P=0.67; Figure 2C). However, significant differences were observed in regional axillary recurrence (log-rank P=0.03; Figure 2D) and distant metastases (log-rank P=0.04; Figure 2E).

Discussion

In this 5-year retrospective cohort study involving 453 patients undergoing SLNB, we compared outcomes between intraoperative FS and PS analysis. Our results show that PS alone is comparable to FS in terms of DFS and OS, aligning with earlier reports (6,22). Specifically, the 5-year DFS was 95.8% in the PS group and 93.5% in the FS group, showing a statistically significant in favor to the PS method in time-to event analysis. In our analysis, we identified statistically significant differences in LVI and HER-2 status between the FS and PS groups. Specifically, the FS group had a higher rate of LVI, while the PS group had a greater proportion of HER-2 positive tumors. Importantly, despite these differences, adjuvant treatment strategies including chemotherapy, endocrine therapy, radiotherapy, and HER-2-directed therapy were comparable between the two cohorts. Surgical quality indicators, such as margin status, were also balanced. As this was a retrospective cohort study rather than a randomized controlled trial, some degree of imbalance in baseline tumor biology was expected. The median follow-up duration differed between groups, with longer follow-up in the PS group than in the FS group. Although Kaplan-Meier analysis accounts for censoring, unequal follow-up may still affect recurrence detection and the shape of survival curves, especially in a cohort with few events. Overall, these imbalances were minor and unlikely to have introduced significant bias into the survival results. A total of 37 of 453 patients (8.2%) did not receive radiotherapy. Although this represents a minority of the cohort, the proportion may appear relatively high and reflects real-world variation in treatment adherence, including patient preference and concerns regarding potential side effects.

Since the 1980s, both mastectomy and BCS with radiotherapy have been accepted as equivalent local treatments for early-stage breast cancer (23). Recent studies further suggest that BCS with adjuvant radiotherapy may even offer improved survival over mastectomy (24-26). Complementing surgical treatment, accurate axillary staging is critical for tailoring adjuvant therapy and optimizing outcomes. The ACOSOG Z0011 trial marked a paradigm shift in axillary management, concluding that SLNB alone is sufficient for patients with one or two metastatic SLNs undergoing BCS with radiation (6). Follow-up studies confirmed that 10-year OS, DFS, and regional control were comparable between SLNB and ALND, with both arms exceeding 90% 5-year survival (19,27,28). Several recent meta-analyses and reviews support our findings. A large 2023 meta-analysis by Bharath et al. confirmed that FS and touch imprint cytology offered lower diagnostic accuracy compared to PS, especially for micrometastases (15). Similarly, Elshanbary et al. reported that FS had a sensitivity of only ~70%, and its omission did not significantly affect oncologic outcomes (14). The results also align with updated ASCO guidelines, which recommend against routine intraoperative evaluation of SLNs if patients meet Z0011 criteria (1,19). An interesting observation in our data was the slightly higher incidence of regional recurrences and distant metastases in the FS group, possibly attributable to selection bias. Although rare, late metastasis occurring beyond 8 years in the FS group raises questions about the long-term reliability of intraoperative assessments. This late recurrence trend was also observed by Carleton et al. (29), suggesting the need for more extended follow-up in SLNB-based studies.

When examining recurrence patterns, our study demonstrates that both local and regional events were exceedingly rare across both FS and PS groups. Local recurrence occurred in only 0.9% of FS patients and 1.3% of PS patients, showing no statistically significant difference, where omission of ALND did not increase locoregional recurrence at 10 years (6,30). In our cohort, regional recurrence was observed only in the FS group (0.9%) and not in the PS group. Although this difference was not statistically significant due to the very low absolute event numbers, the pattern aligns with the consistently low axillary failure rates reported in Z0011. Importantly, our data confirm that intraoperative FS does not add measurable benefit in preventing axillary recurrences compared to PS alone. More recently, the INSEMA trial further advanced this concept by showing that even complete omission of SLNB in clinically and radiologically node-negative patients did not lead to excess regional recurrences when BCS and whole-breast irradiation were applied (31).

The long-held rationale for using FS has been to prevent second surgeries. However, concerns have been raised about the false negative rate of FS when compared to the final result, which varied from 9% to 33% (32,33). Discordance of numbers of positive nodes reported by the intraoperative result and the PS have also been reported (34). Previous studies at our center supports the claim that additional FS may not yield significant value in terms of reoperation prevented for early-stage breast cancer (20,21,35). Our study found notable differences in DFS, regional recurrence, and distant metastases between the two groups, with the FS group experiencing more events than the PS group.

Our findings also resonate with the evolving paradigm in axillary management, notably influenced by the Sentinel node versus Observation after axillary UltraSound (SOUND) trial. This randomized study demonstrated that in clinically node-negative patients (cT1N0) with negative axillary ultrasound, omission of SLNB did not compromise DFS or OS, highlighting the potential of axillary ultrasound as a reliable tool for nodal staging (36). Nevertheless, several limitations should be acknowledged. First, the trial initially excluded patients with higher-risk breast cancers, including those with high tumor grade, HER-2-positive, or triple-negative subtypes, which limits its generalizability to modern practice. Second, some subsequent analyses applying the SOUND criteria have faced challenges with relatively small sample sizes and limited long-term follow-up, restricting conclusions on late recurrences or mortality. Third, the omission of SLNB eliminates pathological nodal information, which may influence adjuvant treatment decisions, such as chemotherapy or targeted therapy selection. Finally, the trial was registered relatively late and did not include early interim analyses, raising concerns regarding transparency of reporting (36).

It is also important to revisit the original rationale for performing intraoperative FS during SLNB. The purpose of FS was to avoid reoperation by allowing immediate completion axillary dissection if more than two positive sentinel nodes were detected. However, data show that the proportion of patients with ≥3 positive sentinel nodes is low (2–6%), limiting the practical yield of intraoperative FS to avert reoperation: e.g., only 6% had ≥3 positive SLNs in a large series and modern cohorts report about 2–3% (37,38). As such, the clinical benefit of FS is limited. Moreover, intraoperative FS typically prolongs operative/anesthesia time and adds cost, whereas data show that reducing or omitting FS shortens operations and lowers costs without worsening outcomes, including in resource-limited settings (20,21). Taken together, these considerations suggest that while the SOUND trial underscores the role of high-quality axillary imaging in reducing surgical interventions, the more practical and broadly applicable step in current practice is omission of intraoperative FS in well-selected, clinically and radiologically node-negative patients consistent with ACOSOG Z0011 criteria.

The limitations of this study include the use of data from a single center with a limited sample size, which may affect the generalizability of the findings. As the data were extracted from real-world clinical practice, the lack of randomization between patients with and without FS introduces the potential for confounding factors. The number of recurrence events was low relative to the number of candidate covariates; therefore, the adjusted Cox model may have been vulnerable to overfitting, and these estimates should be interpreted as exploratory rather than definitive. Although our team made efforts to minimize loss to follow-up, we acknowledge that a small number of patients with incomplete follow-up may have influenced the results. Nevertheless, our findings suggest that omitting FS in favor of PS does not compromise oncologic safety and may streamline surgical workflows.

Conclusions

Omission of intraoperative FS in selected patients meeting with ACOSOG Z0011 criteria was not associated with worse oncologic outcomes. Despite baseline differences between groups, long-term DFS and recurrence patterns were comparable. This approach is consistent with global trends and modern evidence-based practices, supporting de-escalation of axillary surgery without compromising oncologic safety.

Acknowledgments

This manuscript has been previously published in the Research Square preprint. We would like to declare that generative AI (Chat GPT-3.5) was used solely for assistance in checking and refining the English language in this manuscript. The authors entirely generated the content, ideas, and findings presented in the manuscript without AI assistance.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2026-0234/rc

Data Sharing Statement: Available at https://gs.amegroups.com/article/view/10.21037/gs-2026-0234/dss

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2026-0234/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-2026-0234/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. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was conducted at King Chulalongkorn Memorial Hospital, and the study protocol was reviewed and approved by the Institutional Review Board of the Faculty of Medicine, Chulalongkorn University (COA No. 0985/2025). Individual consent for this retrospective analysis was waived.

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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