Impact of intraoperative radiotherapy vs. whole-breast external beam radiotherapy for early breast cancer: a propensity score matching study based on SEER database

Introduction

Female breast cancer surpassed lung cancer to become the most prevalent form of cancer in 2020. It is the leading cause of both newly diagnosed cancer cases and cancer-related deaths among women worldwide (1,2). The advancements in screening methods contribute to an increasing amount of breast cancer detected at an early stage (1). For patients with early breast cancer, breast-conserving surgery (BCS) followed with whole-breast external beam radiotherapy (WBRT) remains the primary treatment, which is demonstrated to be a replacement to mastectomy. If adjuvant chemotherapy is administered, WBRT is typically performed 2–4 weeks after the last chemotherapy; otherwise, patients usually receive WBRT in 8 weeks after lumpectomy alone (3,4). However, this delay may result in the loss of the optimal timing for radiotherapy. Additionally, some disadvantages of WBRT like long treatment cycle, high treatment cost, and adverse events, are related to patient’s omission of adjuvant radiotherapy and increase of local recurrence (5).

To address these limitations, the past two decades have witnessed a growing interest in accelerated partial breast irradiation (APBI) as a more targeted and efficient alternative to WBRT. Among the various APBI techniques, intraoperative radiotherapy (IORT) has gained attention for its ability to deliver a single high-dose fraction of radiation directly to the tumor bed during surgery. This approach eliminates the need for postoperative radiation sessions, shortens the overall treatment time, and directly targets the site most prone to recurrence, thereby theoretically enhancing locoregional control while minimizing radiation exposure to healthy tissue (6). Meanwhile, several studies have demonstrated that IORT is not inferior to WBRT in terms of cancer-related mortality, including 5- and 10-year survival rates for early breast cancer patients (7,8). Despite its advantages over WBRT, one major concern has existed that in theory occult foci of cancer in remote areas of the breast stay untreated. Indeed, prospective trials have reported that IORT is involved with a higher likelihood of local recurrence (9,10). For instance, the TARGIT-R trial, which included 667 early-stage patients with a median follow-up of 5.1 years, reported an overall recurrence rate of 6.6% for ipsilateral breast tumors, with recurrence rate of 8% for those patients who underwent IORT (9). Consequently, the selection of appropriate patients for IORT remains a key and heated issue. Large-scale population-based analyses can provide valuable real-world insights that complement randomized trial findings. Leveraging Surveillance, Epidemiology, and End Results (SEER) database, maintained by the National Cancer Institute, allows for comparative effectiveness research across diverse populations and treatment modalities in real-world settings. This study aimed to compare the survival outcomes of IORT vs. WBRT in patients with early-stage breast cancer using propensity score matching (PSM) to reduce potential selection bias in the SEER cohort. Our findings may help refine patient selection for IORT and inform evidence-based guidelines for its use in clinical practice. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-52/rc).

Methods

Patients selection and data source

In this study, we acquired data from the SEER database of National Cancer Institute. The SEER database contains information about patient demographics and cancer characteristics from 18 cancer institutions that covers nearly 28% of the population in the United States. We accessed the data using SEER*Stat 8.4.2 software. Since all patients were deidentified in the database, no informed consent was required. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

The enrolled patients were diagnosed with early-stage breast cancer who received radiotherapy from 2010 to 2019. The inclusion criteria for our study were as follows: (I) pathologically confirmed early-stage breast cancer of invasive ductal carcinoma, with positive estrogen receptor (ER) (staged T1–2N0M0); (II) received IORT or WBRT; (III) age ≥18 years old; and (IV) no concurrent cancer.

PSM was used to match patients in a 1:4 ratio, with matching covariates including marital status, year of diagnosis, age, race, grade, T stage, ER, progesterone receptor (PR), human epidermal growth factor receptor 2 (HER2), and chemotherapy. Ultimately, a total of 83,474 patients were included in the analysis.

Study variables

Baseline characteristics, such as year of diagnosis, sex, age, tumor grade, stage, race, marital status, pathological characteristics, treatment, and patient survival, were analyzed. The primary endpoints of this study were cancer-specific survival (CSS) and overall survival (OS). CSS was defined from the date of diagnosis to the date of death caused by breast cancer. And OS was defined from the date of diagnosis to the date of death caused by any event. For patients who survived, their follow-up was defined until the date of their last follow-up.

Statistical analysis

All statistical analyses were performed using SPSS 22 statistical software (SPSS Inc., Chicago, IL, USA). The Chi-squared test was used to compare categorical variables between groups. Survival outcomes before and after matching were evaluated using the Kaplan-Meier method. Univariate and multivariate Cox proportional hazards regression analyses were conducted to identify risk factors. A significance level of P<0.05 was considered statistically significant, and all P values were two-sided.

Results

The median follow-up of our study cohort was 57 (interquartile range, 12–119) months. As shown in Figure 1, this study utilized data from the SEER database, including a total of 112,656 patients diagnosed with first, primary breast cancer who underwent BCS from 2010 to 2019. In total, we excluded 14 patients with bilateral or multifocal breast cancer, 77 patients with borderline or unknown ER status, 291 patients with borderline or unknown PR status, 5,127 patients who received neoadjuvant chemotherapy or unknown chemotherapy, 23,046 patients who did not receive IORT or WBRT, 509 patients with unknown tumor grade, 78 patients with pathologically confirmed in-situ carcinoma, and 470 patients with unknown race. Finally, a total of 83,474 patients were included in this study.

Figure 1 Flow chart of enrolling patients in this study. ER, estrogen receptor; HER2, human epidermal growth factor receptor 2; IORT, intraoperative radiotherapy; M, metastasis; N, node; PR, progesterone receptor; T, tumor; WBRT, whole-breast external beam radiotherapy.

Figure 2 illustrates a significant unbalance in the percentage of annual patients who received IORT (n=1,760) and WBRT (n=81,714). Due to the small number of patients in the IORT group, they were matched with a 1:4 PSM ratio with patients who underwent WBRT.

Figure 2 Percentage of early-stage patients who received radiotherapy from 2010 to 2019. IORT, intraoperative radiotherapy; WBRT, whole-breast external beam radiotherapy.

The baseline information and clinical characteristics are presented in Table 1. For the IORT group, the majority of patients were married (59.9%), White race (85.4%), and aged >65 years (47.6%). As for grading and staging systems, most patients were in grade I/II (89.0%) and had a stage T1c tumor (43.9%). The IORT group had a higher percentage of patients with ER-positive status (98.6%) and PR-positive status (90.5%), and a higher percentage of patients with HER2-negative status (94.7%). Among all patients in both groups, the majority did not receive chemotherapy, or it was unclear whether they received chemotherapy. After matching, 8,800 patients in total were selected for analysis, consisted of 7,040 patients in the WBRT group and 1,760 patients in the IORT group. And there was no difference of clinical characteristics between the two groups (Table 2).

Overall, regardless of before and after PSM, Kaplan-Meier analysis showed that there was no difference of CSS and OS between the IORT and WBRT group (Figure 3). Univariate and multivariable Cox analyses were conducted to identify factors influencing CSS and OS. The univariate analysis indicated that IORT patients had better CSS and OS than WBRT patients [CSS: hazard ratio (HR) =1.34, 95% confidence interval (CI): 0.80–2.22; OS: HR =1.11, 95% CI: 0.82–1.50], but the differences were not statistically significant (P≥0.05). Additionally, the univariate analysis revealed that age and tumor stage (T stage) were significantly correlated with CSS and OS. ER, PR, HER2 status, and grade were significantly associated with CSS (P<0.05) (Figure 4).

Figure 3 The survival curves of early-stage breast cancer patients before and after PSM. (A) CSS curves before PSM. (B) OS curves before PSM. (C) CSS curves after PSM. (D) OS curves after PSM. CSS, cancer-specific survival; IORT, intraoperative radiotherapy; OS, overall survival; PSM, propensity score matching; WBRT, whole-breast external beam radiotherapy.

Figure 4 Forest plot of CSS and OS were analyzed by the univariate Cox proportional hazard models before PSM. CI, confidence interval; CSS, cancer-specific survival; ER, estrogen receptor; HER2, human epidermal growth factor receptor 2; HR, hazard ratio; IORT, intraoperative radiotherapy; OS, overall survival; PSM, propensity score matching; PR, progesterone receptor; ref., reference; T, tumor; WBRT, whole-breast external beam radiotherapy.

Both clinically and statistically significant factors were included in the multivariate analysis (Figure 5). The multivariate analysis demonstrated that there was no significant difference in CSS or OS between the IORT group and the WBRT group (CSS: HR =1.23, 95% CI: 0.74–2.05; OS: HR =1.3, 95% CI: 0.96–1.75). However, ER, PR, and HER2-positive status were associated with a better CSS and OS (ER: HR =0.73, 95% CI: 0.57–0.92; PR: HR =0.60, 95% CI: 0.52–0.69; HER2: HR =0.61, 95% CI: 0.51–0.74) (all P<0.01). Moreover, older patients and those with low-grade tumor had significantly worse CSS compared to younger patients and those with high-grade tumor (both P<0.01). Patients diagnosed with stage T2, other than T1a, T1b, or T1c, had a worse survival compared to those patients with stage T1mic tumor. Besides, chemotherapy was indicative of a worse survival. The Cox analysis model was not constructed in the after-PSM cohort because few outcome events were identified.

Figure 5 Forest plot of CSS and OS were analyzed by the multivariate Cox proportional hazard models before PSM. CI, confidence interval; CSS, cancer-specific survival; ER, estrogen receptor; HER2, human epidermal growth factor receptor 2; HR, hazard ratio; IORT, intraoperative radiotherapy; NA, not available; OS, overall survival; PSM, propensity score matching; PR, progesterone receptor; ref., reference; T, tumor; WBRT, whole-breast external beam radiotherapy.

Discussion

BCS followed with WBRT has been universally recognized as the standard care for early breast cancer (11,12). As a means of APBI, IORT is an approach that enables a precisely targeted and high-dose radiotherapy delivery to the tumor bed during BCS before wound closure. Many researchers believe that IORT can serve as a treatment option as effective as WBRT with more advantages like decreased treatment duration, precise irradiation field, and reduced damage to the surrounding normal tissues (13,14). Several consensus statements on the patient selection have been established (15,16). Nevertheless, their application has elicited a skeptical response from studies regarding whether the eligibility criteria for interstitial brachytherapy (BT), the most common APBI modality, is suitable for IORT (17-19). Therefore, more studies are warranted to optimize the patient selection for IORT to guarantee good results. In this study we attempted to gather a substantial number of data on early breast cancer patients from the SEER database with the goal of examining the survival outcomes of IORT and WBRT, as well as investigating the relevant factors that influence the prognosis of breast cancer patients.

The American Brachytherapy Society consensus suggests that whatever IORT technique is used, as a monotherapy for breast cancer patients after BCS, IORT should not be offered outside prospective clinical trials (20). This cautious recommendation is based on two large randomized trials that compared the roles of WBRT and IORT in early breast cancer. The TARGIT-A study enrolled 3,451 breast cancer patients who were randomly allocated to receive either WBRT or IORT (with 50 kV X-rays, 20 Gy to the surface). Among them, 20% of patients after lumpectomy were identified with high-risk factors and then received WBRT, with IORT deemed as a boost to the tumor bed. Despite the higher local recurrence was detected in the IORT group within 3 years, the long-term follow-up showed that there turned out to be a similarity in 5-year local recurrence and survival outcome between the two arms (7). However, concerns arised about the non-inferiority study design and subgroup analysis (21). In the ELIOT study, 1,305 early breast cancer patients were randomized to undergo IORT (21 Gy IORT with electrons) or WBRT. After a long-term follow-up, there was no significant difference in survival between the IORT and WBRT groups (5-year survival rate: 96.8% vs. 96·8%, respectively; 10-year survival rate: 90.7% vs. 92.7%, respectively). Although an absolute excess of 54 ipsilateral breast tumor recurrence was observed in the IORT group as compared to WBRT with a HR of 4.62 (95% CI: 2.68–7.95; P<0.0001), a subgroup analysis found an outstandingly low incidence of local recurrence in selected low-risk patients, characterized by tumor size, grade, molecular subtype, and Ki67 index (3,17). While our data show comparable long-term survival between IORT and WBRT, the higher local recurrence risk associated with IORT reported in TARGIT-A and ELIOT, which was highlighted by ASTRO, remains a key concern (18,19). We emphasize that our findings support IORT as a potential option for carefully selected low-risk patients. However, the definition of low-risk patients needs to be explored in further studies. A previous large-cohort research that retrospectively analyzed early-stage breast cancer patients from the SEER database confirmed the similarity in survival between the two groups (22). Consistently, our study acquired the latest data from the SEER database and also found no significant difference in OS and CSS between patients in the IORT and WBRT groups during the 10-year follow-up.

Undeniably, it is crucial to screen the appropriate patients off-protocol that could truly and safely benefit from IORT. First of all, it is testified by a previous study that early breast cancer patients with positive hormone receptor status received IORT had better survival (18). In addition, another study showed that age was an essential factor associated with local control (23). NSABP B-17 and B-24 trials, two large randomized controlled clinical trials with 15 years of follow-up, found that compared with patients aged over 65 years old, patients younger than 45 years old had a 2.1-fold increased risk of recurrence after BCS (23). Our analysis indicated worse CSS in elderly patients. This discrepancy may be attributed to radiotherapy-related complications, inherent selection bias or confounding variables in the SEER database. While the CALGB 9343, PRIME II, and LUMINA trials have explored the possibility of omitting radiotherapy in elderly patients with early-stage breast cancer, our study suggest that radiotherapy may have a detrimental impact on elderly breast cancer patients, warranting further attention and investigation. Besides, tumor size and grade were also important indicators for breast cancer mortality (24). In particular, a retrospective research recommended grade as a key factor to the low-risk group “suitable” for IORT (25). Our results also showed that the grade and status of ER, PR, and HER2 were significantly correlated with CSS, while OS was relatively worse in stage T2 and elderly patients. Our results suggest that the HER2 positivity as an exclusion for IORT may not be justified. Notably, though it is consistent in the multivariate analysis of our study, the univariate analysis showed a contradictory finding, that was a worse CSS but better OS in the chemotherapy group compared with the no chemotherapy group, which was exactly presented in another SEER-based study (3). Obviously, evidence-based data have demonstrated conclusively that patients with high-risk indicators like grade III/IV, hormone receptor negative, and HER2 positive, tend to receive chemotherapy and predict a relatively poor prognosis (26). Meanwhile, another explanation is the uneven distribution of cases between the two groups of patients in our study. Owing to few outcome events in the IORT group, we were unable to perform Cox regression analysis in the after-PSM cohort. Furthermore, IORT was recognized as a safe approach with no excess acute local morbidity including delayed wound healing or infection (27). By contrast, general increases in breast density and skin thickening were more common in the WBRT group, while mammographic scar or calcification in postoperative site were similar between the two groups (28). Due to the information limitation of SEER database, we failed to analyze the influencing factors of local recurrence or the treatment-related adverse reaction.

Despite being a large-cohort nationwide retrospective research based on the latest data from the SEER database, there are some limitations in this study. First, due to a large proportion of patients included in our study, we adjusted as many as confounders through multivariate analysis, PSM, and other methods to balance the bias between the two groups, but the discrepancy in the sample size and inherent bias call for cautions to the results in this observational study. Secondly, given the limitations of experience, sophisticated equipment and facilities, the wide utilization of IORT has encountered significant challenges, let alone the already low mortality and recurrence rates observed in early breast cancer. Hence, these aspects constrain the statistical comparison between IORT and WBRT. Thirdly, SEER database dose not contain details in radiotherapy about the techniques, doses, and periods, as well as information like margin status and re-excisions, all of which are important factors correlated with survival. The data about local recurrence are absent in the SEER database.

Conclusions

In general, the long-term survival of IORT is not inferior to that of WBRT for early-stage breast cancer. This study showed no significant difference in CSS and OS between IORT and WBRT. ER, PR positive, HER2 negative, and low-grade were indicators for better survival while age over 50 years and stage T2 were correlated with worse survival. The poorer prognosis observed in older patients may, in part, be attributed to radiotherapy-related complications. These factors should be investigated in further prospective case-controlled trials to optimize the patients selection for IORT.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-52/rc

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2025-52/prf

Funding: This study was supported by grants from the National Natural Science Foundation of China (No. 82173232), the Natural Science Foundation of Guangdong Province (Nos. 2023A1515010304 and 2022A1515012497), the Guangzhou Science and Technology Program (No. 202201010807), the Project of Traditional Chinese Medicine Bureau of Guangdong Province (No. 20221075), and the Noncommunicable Chronic Diseases-National Science and Technology Major Project (No. 2023ZD0502300).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2025-52/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

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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