Survival benefit of surgery for inflammatory breast cancer patients

Introduction

Inflammatory breast cancer (IBC) is considered as the most aggressive subtype of breast cancer, accounting for approximately 2–4% of all breast cancer cases in the United States (1). It causes 7–10% of breast cancer-related deaths in Western countries (1), as well as 4,000 deaths per year in the United States (2). Lee and Tannenbaum first described this specific subtype of breast cancer (3) and it is characterized by the rapid onset of skin changes resulting from the embolism of the tumor into the lymphatic vessels of the skin (4). Compared to non-IBC, IBC has a worse prognosis primarily due to its high risk of early distant metastasis (5). Therefore, it is crucial to develop the precise therapeutic strategies for IBC patients.

Prior to the advent of systemic chemotherapy, using either surgery alone or surgery in conjunction with radiotherapy to manage IBC led to local recurrence rates of up to 50% and median survival times of less than 15 months (6). The median overall survival (OS) of patients with IBC is 4.75 years, while patients with non-IBC breast cancer have a median OS of 13.40 years according to the report (7). Given the high risk of metastatic relapse and overall poor prognosis, the value of surgery in the treatment of IBC remains controversial, although many centers incorporate it as part of a multimodal approach. Meanwhile, there is a scarcity of research studies systematically evaluating the impact of surgery on the prognosis of this low-incidence malignancy. In the past, mastectomy as a standalone procedure did not result in any survival advantage as the main type of treatment (8). A study conducted at the Royal Marsden Hospital found that surgery, when combined with radiation therapy, led to increased median progression-free survival (PFS) for patients, but these differences lacked statistical significance (9). However, in the case of patients who respond well to neoadjuvant chemotherapy, surgery has been shown to improve local control rates and survival outcomes (10). Further systematic investigation is warranted to ascertain whether surgery impacts the prognosis of patients with IBC positively.

In this study, we conducted an analysis utilizing the Cox proportional hazards models after propensity score matching (PSM). This study aims to assess the impact of surgical intervention as well as other variables on the prognosis of patients with IBC, and to enhance comprehension of the effectiveness of surgical procedures in a multimodality approach. We present this article in accordance with the STROBE reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-2024-561/rc).

Methods

Patients

Patients with IBC were selected from the Surveillance, Epidemiology, and End Results (SEER)-17 Registries database [2000–2020] using National Cancer Institute (NCI)’s SEER*Stat software (version 8.4.2). Histologic and site codes from the International Classification of Diseases for Oncology, Third Edition (ICD-O-3) were employed to analyze patients with IBC, as previously documented. IBC histology was identified with SEER ICD-0-3 codes: 8530-3. The tumor-node-metastasis (TNM) staging data were obtained using to the following codes: Derived American Joint Committee on Cancer (AJCC) Stage Group (IIIB–IIIC), 6^th Ed, Derived AJCC T, 6^th Ed, Derived AJCC N, 6^th Ed, and Derived AJCC M, 6^th Ed. All patients who presented with tumor (T) status other than T4d status, or those with M1 status, or those with an unknown primary site of surgery (code: 98-99), or those with incomplete dates, were excluded from the study. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments.

Study variables

The SEER database provided the following clinicopathological factors: age at diagnosis, marital status, race, TNM stage, tumor stage, tumor grade, estrogen receptor (ER) status, progesterone receptor (PR) status, human epithelial growth factor receptor-2 (HER2) status, survival data, and treatment information such as primary site of surgery, chemotherapy, and radiotherapy. To facilitate further analysis, categorical factor variables were transformed into continuous numeric variables by calculating the average of each age range of the patients. For patients above 85 years old, they were considered to be 85 years old. We would like to investigate the role of surgical treatment in IBC patients. The main outcome of this study was determined by examining patients’ survival status and time in months.

Statistical analysis

The t-test or χ²-test were used to compare the basic characteristics of patients in surgery and non-surgery groups. In order to determine the factors related to improved OS, we conducted a study using univariate and multivariate Cox proportional hazard models. Potential risk factors were initially identified through univariate analysis, and then we further analyzed with multivariate analysis to confirm their significance. The findings were presented in terms of hazard ratios (HRs) with corresponding 95% confidence intervals (CIs). In order to achieve a balance of covariates, a 1:1 PSM was employed to match patients in the surgical group with those in the non-surgical group. The matching factors included age, race, marital status, node (N) status, stage status, grade status, ER, PR, HER2, chemotherapy and radiotherapy. The matching process is guided by a ratio value of 1 and a caliper value of 0.02. Then, we conducted subtype analysis through Cox proportional hazard models (without model selection) and Kaplan-Meier (KM) estimators to determine the potential impact of surgical treatment in different conditions and subgroups. All analyses were done using R-studio (version 4.2.1) and R package survival (v3.3-1), rms (v6.7-0), survminer (v0.4.9), MatchIt (4.5.0), cobalt (v4.5.1), and EValue (4.1.3).

Results

Patient characteristics

A total of 2,473 IBC patients diagnosed between 2000 and 2020 were evaluated from the SEER database (Figure 1). The surgery group comprised 2,175 patients while the non-surgery group consisted of 298 patients (Table 1). The two groups differed significantly in various characteristics. Firstly, in terms of demographic factors, the non-surgical group had a lower proportion of white individuals and a higher proportion of black individuals (white: 75.2% vs. 81.8%; black: 17.8% vs. 12.8%). Additionally, the non-surgical group had a lower percentage of married patients (40.3% vs. 53.6%). In terms of hormone receptor status, the non-surgical group had lower rates of ER-positive (31.2% vs. 46.3%) and PR-positive (24.2% vs. 34.9%) compared to the surgical group. However, the non-surgical group had a higher proportion of HER2-positive cases than the surgical group (7.7% vs. 5.7%). Furthermore, a higher percentage of non-surgical patients did not receive chemotherapy (23.8% vs. 12.0%) or radiation therapy (78.5% vs. 36.0%) compared to the surgical group. These findings highlighted the differences between the non-surgical and surgical groups, indicating potential disparities in treatment modalities and outcomes.

Figure 1 Flowchart of this study. ER, estrogen receptor; HER2, human epithelial growth factor receptor-2; IBC, inflammatory breast cancer; N, node; PSM, propensity score matching; SEER, Surveillance, Epidemiology, and End Results; T, tumor.

Comparisons of survival outcomes between the surgery group and the no-surgery group

The Univariate analysis revealed significant correlations between age, race, marital status, N status, stage status, grade, ER status, PR status, HER2 status, chemotherapy, surgery and outcomes (survival status and survival time) (Table 2). Moreover, all significant factors identified from the multivariable Cox analysis were included in the Cox regression model. Post-surgery, patients with IBC showed higher OS rates (HR =0.50, 95% CI: 0.43–0.57, P<0.001) (Table 2). To minimize bias, a 1:1 PSM analysis was performed between the patient groups. The caliper value for the PSM matching was set at 0.02. Ultimately, 522 patients were evaluated, with each subgroup consisting of 261 patients (Table 3). After PSM, P values of all covariates were greater than 0.05, indicating significant overlap in the propensity scores between the two groups and PSM method succeed in balancing the covariates (Table 3). The multivariable analysis of the propensity score-matched groups revealed significant associations between age, race, N status, ER status, HER2 status, surgery, chemotherapy, and OS (Table 4). Within the matched population analysis, patients derived significant benefits from surgery (HR =0.51, 95% CI: 0.42–0.62, P<0.001) (Table 4).

Subgroup analysis after PSM

Based on the covariates significant in multivariate Cox analysis, subgroup analysis was conducted to evaluate the impact of surgical treatment on patients in different conditions and subgroup. In the white (HR =0.57, 95% CI: 0.45–0.71, P<0.001, Figure 2), black race (HR =0.48, 95% CI: 0.31–0.73, P<0.001, Figure 2) group and other races (HR =0.45, 95% CI: 0.20–0.99, P=0.047, Figure 2), surgical treatment reduced the risk of OS. Surgery was associated with a lower risk of death for N0 (HR =0.46, 95% CI: 0.31–0.67, P<0.001, Figure 2), N1 (HR =0.56, 95% CI: 0.40–0.77, P<0.001, Figure 2), N2 (HR =0.39, 95% CI: 0.22–0.69, P=0.001, Figure 2). While surgery cannot alter the OS of patients with N3 status (HR =0.71, 95% CI: 0.49–1.00, P=0.06, Figure 2). For different N stages, we also plotted the KM curves and calculated the P values using the log-rank tests (Figure S1). The results were consistent with the Cox regression analysis results. In order to learn about the role of surgery in patients with different stage and grade, patients were divided into grade I–II, and III–IV, and KM curves analysis was conducted. The results revealed that surgery was associated with a reduced risk of mortality in grade I–II (P<0.001) and grade III–IV (P<0.001) (Figure 3A,3B). Furthermore, surgery was found to be an independent prognostic factor for stage IIIB patients (P<0.001, Figure 3C). However, in stage IIIC, surgery did not show a significant difference in the prognosis for patients (P=0.07, Figure 3D). Subsequently, significant differences were observed in patients who underwent surgical treatment in terms of ER positivity or negativity (ER⁻: HR =0.53, 95% CI: 0.41–0.70, P<0.001; ER⁺: HR =0.60, 95% CI: 0.43–0.84, P=0.003) (Figure 2). Additionally, there were significant changes in outcome for both HER2-negative and HER2-positive patients after surgery (HER2⁻: HR =0.51, 95% CI: 0.30–0.87, P=0.01; HER2⁺: HR =0.46, 95% CI: 0.21–0.98, P=0.043). Moreover, the OS outcomes of patients who received chemotherapy or radiation therapy in addition to surgical treatment were superior to those who did not undergo surgery (chemotherapy, P<0.001; radiation therapy, P<0.001) (Figure 3E,3F).

Figure 2 Forest plot of the association of surgery with overall survival of inflammatory breast cancer patients after propensity score matching in subgroup analyses. *, 0.01≤P<0.05; **, 0.001≤P<0.01; ***, P<0.001. ER, estrogen receptor; HER2, human epithelial growth factor receptor-2; N, node.

Figure 3 Overall survival stratified by surgery in grade I–II subgroup patients (A), grade III–IV subgroup patients (B), stage IIIB subgroup patients (C), stage IIIC subgroup patients (D), chemotherapy subgroup patients (E), and radiation subgroup patients (F).

Discussion

In this study, the PSM method was employed to balance other variables, and multiple Cox regression analysis indicated that surgery improved the OS of IBC patients. These findings underscore the significance of surgical intervention in the management of IBC, highlighting its potential impact on patient outcomes. Moreover, the use of SEER data in this research allows for valuable insights from a comprehensive analysis of a considerable patient population, shedding light on the prognosis and treatment options of this rarely seen and highly challenging form of breast cancer.

Current expert panel guidelines recommend a multimodality approach, receiving systemic chemotherapy before mastectomy and radiation therapy, as the standard treatment strategy (11). Although surgery plays a significant role in multidisciplinary treatment, historical evidence suggests that mastectomy as the sole treatment modality fails to confer any survival benefit to IBC patients (8). Even when studies with relevance do exist, they are often limited by sample constraints, yielding unreliable results. A recent study using the SEER database constructed a prognosis prediction model and identified surgery, response to neoadjuvant therapy (NAT), chemotherapy, breast cancer molecular subtypes, and metastasis (M) stage as top five significant variables (12). In the same period, another Fine-Gray’s model demonstrated that the prognosis for cancer-specific survival was significantly influenced by M stage, N stage, and surgery (13). In a study of The Florida Cancer Registry, the patients receiving chemotherapy without surgical treatment had a poorer outcome than chemotherapy either before or after surgery, or surgery without chemotherapy (14). However, these studies primarily focused on investigating pathological markers of prognosis or exploring prognostic factors for IBC and the results could be affected by confound factors. In our own study, regardless of whether it was performed before or after PSM, in univariate or multivariate analysis, we found that surgery improved patients’ prognosis (P<0.001). This is an encouraging finding, suggesting that surgeons can broaden the indications for surgery and strive for better outcomes in patients with IBC.

Multimodality approach has been adopted in most locations and has improved survival outcomes of IBC patients (15). The standard treatment for locally advanced IBC patients having a good response to neoadjuvant chemotherapy is breast-conserving surgery combined with axillary lymph node dissection, followed by adjuvant radiotherapy and adjunctive endocrine therapy if indicated (16). The innovations of systemic therapy result in rising rates of pathologic complete response in affected breast and the axilla (17). For patients with good response to neoadjuvant chemotherapy, surgery can enhance local control rates and OS (10). A previous study indicated that choosing breast-conserving surgery following NAT represents a practical and safe strategy for patients with cT3–4 breast cancer, without adverse long-term oncological outcomes (18). Among the patients showing response to neoadjuvant chemotherapy, the optimal surgical approach is mastectomy combined with axillary lymph node dissection, resulting in better prognosis for patients with negative surgical margins (19). However, based on a retrospective series involving 232 patients, the addition of surgery to the treatment regimen leads to a significant improvement in locoregional disease control, without significant difference in terms of OS rate or disease-free interval (20). The purpose of these interventions is to reduce the risk of local recurrence and improve OS rates. In this study, chemotherapy improved the survival time and outcomes of IBC patients after PSM in multivariate analysis (HR =0.66, P=0.01). However, after PSM, radiation therapy showed no association with survival events and time in both univariate (P=0.06) and multivariate analysis (P=0.39). Thus, surgeons must exercise caution in determining which patients will benefit from mastectomy, reserving surgery for patients who respond to radiation therapy and chemotherapy to achieve better outcomes. Thus, surgical treatment should carefully select patients who respond positively to radiation therapy and chemotherapy as candidates for mastectomy in order to improve outcomes.

Compared to non-IBC, IBC is distinguished by reduced hormone receptor expression. This correlation with a more aggressive clinical course and lower survival rates is evident (21). Our research findings align with this statement, demonstrating that in both the surgical and non-surgical groups, there were a greater number of ER-negative patients compared to ER-positive patients. In addition, compared to the other group, ER-positive patients significantly improved the survival events and duration of IBC patients. Overexpression of genes related to actin-driven cell migration has been linked to elevated IBC metastasis (22). Additionally, ablation of ERβ in IBC cells contributed to cell migration and activated the gene network regulating actin reorganization and ERβ’s tumor-suppressive function in inhibiting IBC cell dissemination and preventing metastasis was observed (23). Interestingly, some researcher regarded that HER-positive is crucial to survival rate of IBC patient and HR was not considered as a favorable prognostic factor like NIBC (24). Controlling for ER receptors, a recent study found that low expression and absence of HER2 showed marginal differences in clinicopathologic features and outcomes (25). In this study, HER2-positive existed an improved impact on the survival of IBC patients referenced to HER-negative in multivariate analysis after PSM (HR =0.54, P=0.02). In subtype analysis after PSM, HER2 status also had correlation with the prognosis of IBC patients in both positive and negative group. It is imperative for professionals to continue research into the evolution of hormone receptor and HER2 in IBC. Moreover, investigating HR and HER2 could lead to the identification of novel diagnostic markers and targeted therapies, ultimately improving patient care and survival rates. In the context of IBC with HR-positive and triple-negative breast cancer (TNBC) subtypes, incorporating neoadjuvant chemotherapy therapy such as anthracycline and taxane has proven effective (26). Additionally, for HR⁺ patients, extending adjuvant endocrine therapy can diminish the risk of recurrence. The recommended NAT for HER2-postive IBC is a combination of pertuzumab and trastuzumab, which are dual anti-HER2 antibodies, alongside an anthracycline-containing regimen (26).

The main objective of PSM is to equalize the distribution of covariates between the treatment and control groups. This is achieved by replacing multiple covariates with a single score. By adopting a similar approach to randomization, confounding factors in non-randomized studies are mitigated to reduce selection bias. By removing the influence of confounding factors, the PSM method provides a more robust and reliable assessment of the causal relationship between surgical intervention and outcomes. Through PSM method, we could reduce the impact of confounder factors and study more about the role of surgical treatment in multimodality approach of IBC patients. However, PSM method still has some drawbacks. First of all, a major drawback of PSM method is their inability to account for hidden biases, which is similar to other methods used for deriving causal inferences from observational studies (27). What’s more, the sample size in PSM often diminishes because patients who do not match are frequently discarded, which may negatively affect final study conclusions. Also, PSM estimates average treatment effects without considering treatment heterogeneity and personalized medicine is still a long way from being fully realized.

There are several limitations in this study. Firstly, the SEER database does not contain information on surgery-related factors, such as the methods employed and the duration between surgery and diagnosis. Secondly, because of the rarity of IBC and the stringent inclusion criteria applied, our study’s sample size is limited. This limitation necessitates further validation of the model’s reliability. Future research should consider broader inclusion criteria to encompass a more diverse patient population. Additionally, the SEER database has a scarcity of data on IBC patients with distant metastasis (M1), so our study only focused on patients with no distant metastasis (M0). Furthermore, important prognostic factors including lymph node biopsy, Ki-67 expression, bilateral occurrence, anti-tumor immune response, microvascular invasion, and minimally invasive surgery were not considered in this study, introducing potential bias to the results. Ki-67 is a vital marker for tumor proliferation that influences risk stratification and survival outcomes. Similarly, detailed information on lymph node status and surgical management is essential for evaluating treatment efficacy. Their omission may introduce residual confounding and affect the validity of our findings. Future research should address these limitations by incorporating additional data sources, such as hospital registries or multicenter databases, or by conducting prospective studies that include these variables. Differences in the characteristics of surgery such as breast reconstruction, breast-conserving surgery, number of surgeries, and unmeasured confounding factors could also lead to bias in the matching process using PSM. Moreover, the impact of treatment changes over time, as a result of changes in molecular subtypes and pathological identification criteria, remains unclear and requires further investigation. In addition, the lack of data on postoperative complications and sequelae in the SEER database prevents us from assessing the influence of patient comorbidities, complications, and psychological factors on outcomes and survival time, potentially introducing bias as well. Last but not least, we can not obtain quality of life (QoL) data and disease-free survival (DFS) data due to the data availability of SEER-Medicare Health Outcomes Survey (SEER-MHOS) and SEER-Medicare database. In the future, we will integrate these data to conduct an in-depth analysis of the impact of treatment efficacy on QoL, thereby providing a comprehensive evaluation of the prognostic effects of different treatment strategies.

Our results demonstrate that various factors, such as race, surgery, and chemotherapy, play a significant role in the outcomes of patients with IBC. It also highlights the importance of performing surgeries in IBC patients as it improves their OS rates. The PSM analysis further reinforces the positive effect of surgery on patients. The findings underline the need for personalized treatment plans based on clinical characteristics in order to maximize the benefits of surgery for IBC patients.

Conclusions

Patients with IBC who are treated with surgery have better OS outcomes. Therefore, a multimodality approach is recommended for the management of IBC, which involves the use of surgical intervention as the main treatment modality.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-2024-561/rc

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-2024-561/prf

Funding: This study received funding from the National Natural Science Foundation of China (No. 82303078), Natural Science Foundation of Fujian province of China (No. 2024J08318), Xiamen Health and Wellness High-Quality Development Science and Technology Program (No. 2024GZL-GG59), the First Affiliated Hospital of Xiamen University for Excellent Nurturing Program (No. XYP2023004), Talent Introduction Research Foundation of the First Affiliated Hospital of Xiamen University (No. XYJ2024002), and Beijing Medical Award Foundation (No. YXJL-2020-0941-0746).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-2024-561/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.

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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