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Is surgical axillary staging necessary in women with T1 breast cancer who are treated with breast-conserving therapy?

Cancer Communications volume 39, Article number: 25 (2019) Cite this article

Abstract

Background

In the post-Z0011 trial era, the need to perform surgical axillary staging for early-stage breast cancer patients, who are treated with breast-conserving therapy (BCT), is being questioned. We conducted a retrospective cohort study using the Surveillance, Epidemiology, and End Results (SEER) database to evaluate the safety of waiving surgical axillary staging in patients with T1 breast cancer treated with BCT.

Methods

A total of 166,615 eligible patients diagnosed between 2000 and 2012 were divided into staging (sentinel lymph node biopsy or axillary lymph node dissection) and non-staging (no lymph node examined or only needle aspiration biopsy of lymph nodes) groups. Propensity score matching (PSM) was performed to balance disparities between the two groups. Multivariate analysis with the Cox proportional hazards model was used to assess factors related to breast cancer-specific survival (BCSS).

Results

Although the tumor size at time of presentation was decreasing over years, the rate of surgical axillary staging increased from 93.3% to 96.9%. The 5-year BCSS rates of the whole cohort (before PSM) and matched cohort (after PSM) were 98.0% and 97.5%. Within the matched cohort, the BCSS was significantly longer in the staging group than in the non-staging group (P < 0.001). However, surgical axillary staging did not benefit patients who were 50–79 years old, had tumor size < 1 cm, histological grade I disease, or favorable histological types (tubular/mucinous/papillary) in stratified analyses (P > 0.05). Race, marital status, hormone receptors, and chemotherapy were not associated with the favorable impact of surgical axillary staging on BCSS (P > 0.05).

Conclusion

Although surgical axillary staging remains important for T1 breast cancer patients treated with BCT, it might be unnecessary for patients with old age, small tumor, grade I disease, or favorable histological types.

Background

With improvements in breast cancer screening, increasing numbers of patients are being diagnosed at an early stage with reduced axillary lymph node involvement [1]. As such, surgical treatment of primary breast cancer has de-escalated over the last decades, with breast-conserving surgery (BCS) and sentinel lymph node biopsy (SLNB) being increasingly performed over mastectomy and axillary lymph node dissection (ALND) [2]. Currently, ALND is performed only if the result of SLNB is positive [3]. The International Breast Cancer Study Group (IBSCG) 23-01 trial demonstrated no local control or survival advantages associated with ALND, even in women with micrometastatic SLNs [4]. Furthermore, both the American College of Surgeons Oncology Group (ACOSOG) Z0011 trial and the European Organization for Research and Treatment of Cancer (EORTC) AMAROS trial indicated that ALND could be safely omitted in most patients with 1–2 metastatic SLNs [5, 6].

Although SLNB is highly reproducible, accurate, and associated with reduced morbidity, it is not a risk-free procedure [7]. A 4%–14% rate of complications, such as allergic reactions, hematoma, lymphedema, paresthesia, chronic pain, and immobility, still occurs after SLNB [8,9,10,11]. Additionally, the false negative rate of axillary lymph node status predicted by SLNB is 5%–10%, despite the axillary recurrence rate being only 0.3% [3, 12,13,14]. Taken together, the value of surgical axillary staging for early-stage breast cancer treated with breast-conserving therapy (BCT) remains controversial in the current era of personalized medicine.

The shift in the size of breast tumors is believed to be associated with the increasing use of screening mammography [15]. Until 1999, the average tumor size at initial presentation (stage I–III) has decreased by 10% every 5 years for two decades [16]. However, the rates of T1 tumors (≤ 2 cm) remained relatively unchanged for the past 15 years, and the average tumor size was approximately 1.8 cm [17]. Therefore, using the Surveillance, Epidemiology, and End Results (SEER) database, we aimed to investigate the safety of waiving surgical axillary staging in patients with T1 breast cancer who are treated with BCT.

Patients and methods

Data source

We performed a retrospective cohort study using the SEER custom database (http://www.seer.cancer.gov) (with additional datasets of treatment information, released in April 2017) from the US National Cancer Institute. The SEER database currently includes incidence and survival data collected from 18 population-based cancer registries, which covers approximately 28% of the US population [18].

Female patients diagnosed with breast cancer between January 1, 2000 and December 31, 2012, who met the following criteria, were deemed eligible: (1) had T1 breast cancer; (2) had breast cancer as the primary cancer; and (3) were older than 18 years. Since the recurrence rate and breast cancer-related death rate are unacceptably high when patients are treated with BCS without radiotherapy [19], meeting the Z0011 eligibility criteria, patients who underwent BCS alone were not included in the present study. Exclusion criteria were as follows: (1) the patient had received neoadjuvant therapy (identified using the codes “CS Tumor Size/Ext Eval” and “CS Reg Node Eval” from the Collaborative Stage Data Set); (2) the patient had other simultaneous primary malignant tumor; (3) the patient did not receive cancer-directed surgery at primary site; (4) the type of surgery was unknown; (5) the number of lymph nodes examined was unknown; (6) the patient had metastatic lymph nodes on needle aspiration biopsy, but did not receive further axillary treatment; (7) the patient was diagnosed at autopsy; (8) the follow-up data were unavailable.

Main variables and endpoints

Using the SEER*STAT software version 8.3.4 (Information Management Services, Inc., Calverton, MD, USA), we extracted demographic (year of diagnosis, age, race and origin, and marital status), clinicopathologic (TNM stage classified according to the 6th edition of the American Joint Committee on Cancer staging system, grade, histological type, estrogen receptor, and progesterone receptor), and therapeutic information (surgery of primary site, radiotherapy, chemotherapy, number of regional nodes examined, and number of metastatic regional nodes), along with survival data (cause-specific death classification and survival duration).

According to the “surgery codes of breast C50.0-C50.9”, breast surgeries were classified into BCS and mastectomy. The “number of regional lymph nodes examined” codes (SEER Program Coding and Staging Manual 2016) were used to divide patients into staging and non-staging groups. In particular, we categorized the tumor histology into four types, namely ductal, lobular, favorable (tubular/mucinous/papillary), and others, according to ICD-O-3 codes. The primary outcome was breast cancer-specific survival (BCSS) [20], which was measured from the date of diagnosis to the date for which “cause-specific death” data were available.

Statistical analysis

Patient characteristics were compared between the staging and non-staging groups using Pearson’s Chi-square test for categorical variables. Temporal trends were assessed using the Cochran–Armitage test. Propensity score matching (PSM) was performed to balance disparities between the two groups. Propensity score for the status of surgical axillary staging was calculated for each patient using multivariate logistic regression, considering all imbalanced factors. We performed a 5-to-1 digit greedy match algorithm at a 1:1 ratio to estimate the propensity score without replacement [21]. Considering that some information (such as endocrine therapy) was not available in the SEER database, we also conducted sensitivity analysis to examine the impact of various levels of hidden bias on the interpretation of treatment effect [22].

The Kaplan–Meier method was used to plot BCSS curves, and log-rank test was performed for comparison of survival. Significant prognostic factors in the univariate analysis were included in the Cox proportional hazards regression model for multivariate analyses. Hazard ratios (HR) from the final models are presented with 95% confidence intervals (CI). Statistical analysis was performed using the SAS version 9.4 software (SAS Institute, Cary, NC, USA) and R version 3.2.0 software (R Foundation for Statistical Computing, Vienna, Austria). Statistical significance was defined as a two-sided P value < 0.05.

Results

Patient characteristics

A total of 406,535 women older than 18 years were diagnosed with T1 breast cancer between January 1, 2000 and December 31, 2012. We identified 166,615 eligible patients who were treated with BCS and radiotherapy. Among them, 160,141 (96.1%) patients who underwent SLNB or ALND were classified into the staging group, and 6474 (3.9%) patients who had no lymph node examination or only needle aspiration biopsy of lymph nodes were classified into the non-staging group (Fig. 1). The proportions of T1mic and T1a tumors increased with years, followed by a significant decrease in the proportion of T1c tumors from 56.2% to 53.5% (P < 0.001) (Fig. 2a). Although the tumor size at presentation was decreasing over years, the rate of surgical axillary staging increased from 93.3% to 96.9% (P < 0.001) (Fig. 2b).

Fig. 1
figure1

Flow diagram of identifying eligible patients with pT1 breast carcinoma diagnosed between 2000 and 2012 from the Surveillance, Epidemiology, and End Results (SEER) database (November 2016 Submission). BCS: breast-conserving surgery, RT radiotherapy

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Fig. 2
figure2

Temporal trends of tumor size and surgical axillary staging in the 166,615 T1 breast cancer patients. a Tumor size distribution; b rate of surgical axillary staging

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Table 1 summarizes the association of surgical axillary staging with other variables. The median ages of patients in the staging and non-staging groups were 60 and 72 years. In the whole cohort, there were more non-Hispanic white, widowed, and older (> 65 years) patients as well as higher proportions of small (T1mic/T1a), well-differentiated (Grade I), and favorable histological types of tumors in the non-staging group (P < 0.001). Additionally, patients in the non-staging group were less likely to receive chemotherapy (P < 0.001). Balance in patient characteristics was achieved after propensity score matching (P > 0.05). Sensitivity analysis showed a Γ value of 1.253, suggesting that the majority of relevant covariates were included with no significant hidden confounder potentially affecting the treatment effects and that all observed covariates had the same chance of assignment to treatment in the two groups in the matched cohort.

Table 1 Characteristics of patients with or without surgical axillary staging
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Multivariate analysis of BCSS

Median follow-up of the matched cohort was 89 months (interquartile range 52–134 months), which was the same as that of the whole cohort. The 5-year BCSS rates of the whole and matched cohorts were 98.0% and 97.5%. As shown in Table 2, BCSS was improved over time, and all the variables were identified to be significantly associated with BCSS in the whole cohort. For the matched cohort, the risk of death from breast cancer in patients with surgical axillary staging was significantly lower than in the non-staging group (HR = 0.70, 95% CI 0.59–0.83, P < 0.001) (Fig. 3a). Patients with an age between 50 and 64 years, T1mic/T1a tumor, grade I disease, positive estrogen receptor (ER) status, and positive progesterone receptor (PR) status had longer BCSS than their counterparts (Fig. 3b–f). The use of chemotherapy did not show a survival benefit in multivariate analysis (HR = 1.29, 95% CI 0.94–1.77, P = 0.115), nor did favorable histological types (HR = 0.99, 95% CI 0.69–1.42, P = 0.966) (Table 2). In addition, American Indian/Alaska native (HR = 4.73, 95% CI 1.16–19.27, P = 0.030) and widowed patients (HR = 1.25, 95% CI 1.01–1.55, P = 0.045) had shorter BCSS relative to other groups (Table 2).

Table 2 Multivariate analysis of BCSS in the whole and matched cohorts
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Fig. 3
figure3

Kaplan–Meier curves of breast cancer-specific survival (BCSS) in the matched cohort. a Surgical axillary staging significantly prolonged the BCSS of patents (P < 0.001). Patients with age between 50 and 64 years old (b), T1mic/T1a tumor (c), grade I disease (d), positive estrogen receptor (ER) (e), and positive progesterone receptor (PR) (f) had longer BCSS than their counterparts (all P < 0.05)

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Stratified analysis of BCSS within the matched cohort

As shown in Table 3, surgical axillary staging significantly prolonged BCSS of patients younger than 50 years (HR = 0.45, 95% CI 0.24–0.86, P = 0.015) or not younger than 80 years (HR = 0.64, 95% CI 0.47–0.86, P = 0.004) (Additional file 1: Figure S1). Patients with smaller tumors (< 1 cm) had similar BCSS between the two groups (P > 0.05). However, for patients with T1c tumors, BCSS was significantly longer in the staging group than in the non-staging group (HR = 0.67, 95% CI 0.54–0.84, P = 0.001) (Additional file 2: Figure S2). The exemption of surgical axillary staging was safe in patients with grade I disease (HR = 0.98, 95% CI 0.66–1.46, P = 0.933) (Additional file 3: Figure S3) or favorable histological types (HR = 0.91, 95% CI 0.47–1.75, P = 0.777) (Additional file 4: Figure S4). Race, marital status, hormone receptors, and chemotherapy were not associated with the favorable effect of surgical axillary staging on BCSS in the stratified analysis (all P > 0.05) (data not shown).

Table 3 Stratified analysis of BCSS in the matched cohort
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Discussion

The risk of lymph node metastasis in patients with ductal carcinoma in situ (DCIS) is estimated to be only 1%–6%, for whom surgical axillary staging is not required according to the National Comprehensive Cancer Network (NCCN) guidelines [23, 24]. In the present study, the rates of lymph node metastasis in patients with T1mic, T1a, T1b, and T1c tumors were 2.8%, 4.5%, 9.3% and 21.0%, respectively. Therefore, it seems reasonable to omit surgical axillary staging for patients with T1mic or T1a tumors. Furthermore, our survival analysis showed no difference in BCSS between staging and non-staging groups in patients with T1mic, T1a, and T1b tumors, whereas surgical axillary staging only prolonged BCSS of patients with T1c breast cancer.

Young breast cancer patients often present with a more advanced stage and aggressive subtypes at diagnosis, resulting in a poorer prognosis [2]. However, there is a paucity of data regarding the safety of treating young women with less aggressive axillary surgery. A randomized trial (INT09/98) was conducted to determine the impact of avoiding axillary surgery in patients with T1N0 breast cancer [25]. In that trial, 517 patients aged 30–65 years with T1N0 breast cancer were recruited between 1998 and 2003 and were randomized to undergo quadrantectomy either with or without ALND. After a median follow-up of 10 years, no difference was observed in overall survival (OS) and disease-free survival (DFS) between the two treatment arms [25]. In the current study, BCSS did not differ between the two treatment arms in patients aged 50–65 years, which is partially consistent with the results of the INT09/98 trial. However, we identified that surgical axillary staging significantly prolonged BCSS in patients younger than 50 years, suggesting that we should still adhere to the current standard treatment for premenopausal patients.

Breast cancer patients older than 65 years tend to have a favorable prognosis and may not benefit from surgical treatment of the axillary lymph nodes [26, 27]. A study began in 1996 recruited 65–80-year-old patients with cT1N0 breast cancer who were randomized to undergo conservative surgery with or without ALND. After 15 years of follow-up, breast cancer-specific mortality and OS did not differ between the ALND and no ALND arms, and the rates of distant metastases were also indistinguishable [28]. However, Sun et al. [26] found that forgoing surgical axillary treatments in women older than 65 years was associated with short OS and BCSS. The controversy among these trials might be attributed to the relatively small sample sizes. Our results showed that it was safe to omit surgical axillary staging in women between 50 and 79 years old. However, we also found that surgical axillary staging significantly prolonged BCSS of patients of at least 80 years old. We speculate that patients of at least 80 years old were less likely to receive standard systemic therapy than younger patients.

Marrazzo et al. [29] indicated that patients with triple-negative breast cancer could be good candidates for BCT without surgical axillary staging. However, in the present study, ER/PR status was not significantly associated with the impact of surgical axillary staging on BCSS. Although adjuvant chemotherapy has been shown to reduce 10-year breast cancer mortality for all subtypes by one-third compared with no chemotherapy [30], patients who were at low risk for recurrence had a small absolute benefit which might be outweighed by long-term toxicities [31]. Consistently, our results showed that chemotherapy did not prolong BCSS of patients with T1 breast cancer either.

Since the importance of surgical axillary staging is still debatable, new ongoing trials, including the Sentinel Node versus Observation after Axillary Ultrasound (SOUND) trial [32] and the Intergroup Sentinel Mamma (INSEMA) trial [33], have been designed to compare SLNB versus observation in cT1-2N0 patients treated with BCT. The SOUND trial, a non-inferiority trial, aimed to recruit 1560 women (780 in each arm), with the primary endpoint being DFS and OS. The INSEMA study planned to randomize patients to either no axillary surgical intervention or SLNB in a 1:4 allocation (1348 patients in no intervention arm). In the present study, each treatment arm in the matched cohort included 5561 patients, and all covariates were comparable after propensity score matching, which was identified as a simulation of randomized clinical trials [20].

Owing to its retrospective nature, the present study had several limitations. Because the SEER database does not have a reliable parameter to distinguish between ALND and SLNB, we assumed that lymph node examination number ≥ 1 represented a formal surgical axillary staging. In general, radiotherapy after BCS is supposed to cover the whole breast with or without regional nodes, which may influence axillary recurrence rates in patients with low-volume axillary disease [6]. In the present study, all patients underwent BCT. However, information regarding the extent and dose of irradiation was not available. Additionally, endocrine therapy was not recorded, but we believe that this might have not largely impacted the results of this study because the majority of patients with early-stage breast cancer who completed appropriate locoregional treatment were likely to undergo standard systemic therapy [34].

In terms of strong preconceptions on the potential therapeutic benefit of axillary surgery, many patients and physicians are unwilling to take the risk for choosing less aggressive surgical management of the axilla, thereby making randomization problematic. Therefore, a large retrospective study might be an ideal design alternative to solve this dilemma [35]. Due to the great disparity in the proportion of patients with or without surgical axillary staging, it is difficult to avoid selection bias. The multivariate model using Cox regression analysis alone may not fully adjust many confounding factors. Therefore, we performed greedy matching techniques to balance all measured covariates in the dataset, which is a pseudo-randomized study design. Further, we used propensity score matching, which is a widely accepted approach for the control of selection bias in observational studies [36].

Conclusions

Due to more effective screening strategies and adjuvant therapies, the potential risks of axillary surgery may now outweigh its potential benefits, especially in early-stage breast cancer patients treated with BCT. Before the results of ongoing clinical trials are announced, findings of the present mono-institutional retrospective study hint a rationale for waiving surgical axillary staging in subgroups of T1 breast cancers, which are characterized as having tumor size < 1 cm, being 50–79 years old, having grade I disease, and favorable histological types. The possibility to de-escalate axillary treatments needs to be further investigated according to the molecular features of the primary tumor, to be more cost-effective and to reduce risks of potentially avoidable morbidity.

Abbreviations

BCT:

breast-conserving therapy

SEER:

Surveillance, Epidemiology, and End Results

SLNB:

sentinel lymph node biopsy

ALND:

axillary lymph node dissection

BCSS:

breast cancer-specific survival

PSM:

propensity score matching

HR:

hazard ratios

CI:

confidence interval

ER:

estrogen receptor

PR:

progesterone receptor

References

  1. 1.

    Zuo T, Zeng H, Li H, Liu S, Yang L, Xia C, et al. The influence of stage at diagnosis and molecular subtype on breast cancer patient survival: a hospital-based multi-center study. Chin J Cancer. 2017;36:84.

    Article  Google Scholar 

  2. 2.

    Cardoso F, Harbeck N, Barrios CH, Cardoso F, Harbeck N, Barrios CH, et al. Research needs in breast cancer. Ann Oncol. 2017;28:208–17.

    CAS  PubMed  Google Scholar 

  3. 3.

    Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Costantino JP, et al. Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol. 2010;11:927–33.

    Article  Google Scholar 

  4. 4.

    Galimberti V, Cole BF, Zurrida S, Viale G, Luini A, Veronesi P, et al. Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23-01): a phase 3 randomised controlled trial. Lancet Oncol. 2013;14:297–305.

    Article  Google Scholar 

  5. 5.

    Giuliano AE, Ballman K, McCall L, Beitsch P, Whitworth PW, Blumencranz P, et al. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: long-term follow-up from the American College of Surgeons Oncology Group (Alliance) ACOSOG Z0011 Randomized Trial. Ann Surg. 2016;264:413–20.

    Article  Google Scholar 

  6. 6.

    Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJ, Mansel RE, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol. 2014;15:1303–10.

    Article  Google Scholar 

  7. 7.

    Rodier JF, Velten M, Wilt M, Martel P, Ferron G, Vaini-Elies V, et al. Prospective multicentric randomized study comparing periareolar and peritumoral injection of radiotracer and blue dye for the detection of sentinel lymph node in breast sparing procedures: FRANSENODE trial. J Clin Oncol. 2007;25:3664–9.

    Article  Google Scholar 

  8. 8.

    Gartner R, Jensen MB, Nielsen J, Ewertz M, Kroman N, Kehlet H. Prevalence of and factors associated with persistent pain following breast cancer surgery. JAMA. 2009;302:1985–92.

    Article  Google Scholar 

  9. 9.

    Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Ashikaga T, et al. Technical outcomes of sentinel-lymph-node resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial. Lancet Oncol. 2007;8:881–8.

    CAS  Article  Google Scholar 

  10. 10.

    Land SR, Kopec JA, Julian TB, Brown AM, Anderson SJ, Krag DN, et al. Patient-reported outcomes in sentinel node-negative adjuvant breast cancer patients receiving sentinel-node biopsy or axillary dissection: National Surgical Adjuvant Breast and Bowel Project phase III protocol B-32. J Clin Oncol. 2010;28:3929–36.

    Article  Google Scholar 

  11. 11.

    DiSipio T, Rye S, Newman B, Hayes S. Incidence of unilateral lymphedema after breast cancer: a systematic review and meta-analysis. Lancet Oncol. 2013;14:500–15.

    Article  Google Scholar 

  12. 12.

    Giuliano AE, Hunt KK, Ballman KV, Beitsch PD, Whitworth PW, Blumencranz PW, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis. JAMA. 2011;305:569–75.

    CAS  Article  Google Scholar 

  13. 13.

    Rao R, Euhus D, Mayo HG, Balch C. Axillary node interventions in breast cancer a systematic review. JAMA. 2013;310:1385–94.

    CAS  Article  Google Scholar 

  14. 14.

    Mansel RE, Fallowfield L, Kissin M, Goyal A, Newcombe RG, Dixon JM, et al. Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC trial. J Natl Cancer Inst. 2006;98:599–609.

    Article  Google Scholar 

  15. 15.

    Welch HG, Prorok PC, O’Malley AJ, Kramer BS. Breast-cancer tumor size, overdiagnosis, and mammography screening effectiveness. N Engl J Med. 2016;375:1438–47.

    Article  Google Scholar 

  16. 16.

    Elkin EB, Hudis C, Begg CB, Schrag D. The effect of changes in tumor size on breast carcinoma survival in the US: 1975–1999. Cancer. 2005;104:1149–57.

    Article  Google Scholar 

  17. 17.

    Fenton JJ, Abraham L, Taplin SH, Geller BM, Carney PA, D’Orsi C, et al. Effectiveness of computer-aided detection in community mammography practice. J Natl Cancer Inst. 2011;103:1152–61.

    Article  Google Scholar 

  18. 18.

    Thomas A, Khan SA, Chrischilles EA, Schroeder MC. Initial surgery and survival in stage IV breast cancer in the United States, 1988–2011. JAMA Surg. 2016;151:424–31.

    Article  Google Scholar 

  19. 19.

    Darby S, McGale P, Correa C, Taylor C, Arriagada R, Clarke M, et al. Effect of radiotherapy after breast-conserving surgery on 10-year recurrence and 15-year breast cancer death: meta-analysis of individual patient data for 10,801 women in 17 randomised trials. Lancet. 2011;378(9804):1707–16.

    CAS  Article  Google Scholar 

  20. 20.

    Worni M, Akushevich I, Greenup R, Sarma D, Ryser MD, Myers ER, et al. Trends in treatment patterns and outcomes for ductal carcinoma in situ. J Natl Cancer Inst. 2015;107:djv263.

    Article  Google Scholar 

  21. 21.

    Austin PC. Optimal caliper widths for propensity-score matching when estimating differences in means and differences in proportions in observational studies. Pharm Stat. 2011;10:150–61.

    Article  Google Scholar 

  22. 22.

    Rosenbaum PR. Observational studies. 2nd ed. New York: Springer; 2002.

    Google Scholar 

  23. 23.

    Intra M, Rotmensz N, Veronesi P, Colleoni M, Iodice S, Paganelli G, et al. Sentinel node biopsy is not a standard procedure in ductal carcinoma in situ of the breast: the experience of the European Institute of Oncology on 854 patients in 10 years. Ann Surg. 2008;247:315–9.

    Article  Google Scholar 

  24. 24.

    Francis AM, Haugen CE, Grimes LM, Crow JR, Yi M, Mittendorf EA, et al. Is sentinel lymph node dissection warranted for patients with a diagnosis of ductal carcinoma in situ? Ann Surg Oncol. 2015;22:4270–9.

    Article  Google Scholar 

  25. 25.

    Agresti R, Martelli G, Sandri M, Tagliabue E, Carcangiu ML, Maugeri I, et al. Axillary lymph node dissection versus no dissection in patients with T1N0 breast cancer: a randomized clinical trial (INT09/98). Cancer. 2014;120:885–93.

    CAS  Article  Google Scholar 

  26. 26.

    Sun S, Hollenbeak C, Leung A. Deviation from the standard of care for early breast cancer in the elderly: what are the consequences? Ann Surg Oncol. 2015;22:2492–9.

    Article  Google Scholar 

  27. 27.

    Rudenstam CM, Zahrieh D, Forbes JF, Crivellari D, Holmberg SB, Rey P, et al. Randomized trial comparing axillary clearance versus no axillary clearance in older patients with breast cancer: first results of International Breast Cancer Study Group trial 10-93. J Clin Oncol. 2006;24:337–44.

    Article  Google Scholar 

  28. 28.

    Martelli G, Boracchi P, Ardoino I, Lozza L, Bohm S, Vetrella G, et al. Axillary dissection versus no axillary dissection in older patients with T1N0 breast cancer: 15-year results of a randomized controlled trial. Ann Surg. 2012;256:920–4.

    Article  Google Scholar 

  29. 29.

    Marrazzo A, Boscaino G, Marrazzo E, Taormina P, Toesca A. Breast cancer subtypes can be determinant in the decision making process to avoid surgical axillary staging: a retrospective cohort study. Int J Surg. 2015;21:156–61.

    Article  Google Scholar 

  30. 30.

    Peto R, Davies C, Godwin J, Gray R, Pan HC, Clarke M, et al. Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials. Lancet. 2012;379:432–44.

    CAS  Article  Google Scholar 

  31. 31.

    Azim HA Jr, de Azambuja E, Colozza M, Bines J, Piccart MJ. Long-term toxic effects of adjuvant chemotherapy in breast cancer. Ann Oncol. 2011;22:1939–47.

    Article  Google Scholar 

  32. 32.

    Gentilini O, Veronesi U. Abandoning sentinel lymph node biopsy in early breast cancer? A new trial in progress at the European Institute of Oncology of Milan (SOUND: sentinel node vs observation after axillary UltraSouND). Breast. 2012;21:678–81.

    Article  Google Scholar 

  33. 33.

    Reimer T, Hartmann S, Stachs A, Gerber B. Local treatment of the axilla in early breast cancer: concepts from the national surgical adjuvant breast and bowel project B-04 to the planned intergroup sentinel mamma trial. Breast Care. 2014;9:87–95.

    Article  Google Scholar 

  34. 34.

    Poleszczuk J, Luddy K, Chen L, Lee JK, Harrison LB, Czerniecki BJ, et al. Neoadjuvant radiotherapy of early-stage breast cancer and long-term disease-free survival. Breast Cancer Res. 2017;19:75.

    Article  Google Scholar 

  35. 35.

    Khozin S, Kim G, Pazdur R. Regulatory watch: from big data to smart data: FDA’s INFORMED initiative. Nat Rev Drug Discov. 2017;16:306.

    CAS  Article  Google Scholar 

  36. 36.

    Austin PC, Grootendorst P, Anderson GM. A comparison of the ability of different propensity score models to balance measured variables between treated and untreated subjects: a Monte Carlo study. Stat Med. 2007;26:734–53.

    Article  Google Scholar 

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Authors’ contributions

Conceptualization: JW and JT; software: CS and ZX; formal analysis: JW and HT; data curation: CS and ZX; writing-original draft preparation: JW, HT and XL; supervision: XW, XX and JT; funding acquisition: JW. All authors read and approved the final manuscript.

Acknowledgements

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

All data analyzed in this study are available from the SEER database (http://www.seer.cancer.gov).

Consent for publication

Not applicable.

Ethics approval and consent to participate

Using publically available SEER database, this study was deemed exempt from the Sun Yat-sen University Cancer Center Institutional Review Board, and individual informed consent was waived.

Funding

This work was supported by the National Natural Science Foundation of China (81402183), as well as Young Investigator Award (YIA201413) and the Medical scientist training program (16zxqk07) from Sun Yat-sen University Cancer Center.

Author information

Author notes

  1. Jin Wang and Hailin Tang contributed equally to this work

Affiliations

  1. Department of Breast Oncology, State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center, No. 651 Dongfeng East Road, Yuexiu District, Guangzhou, 510060, Guangdong, P.R. China

    Jin Wang, Hailin Tang, Xing Li, Cailu Song, Zhenchong Xiong, Xi Wang, Xiaoming Xie & Jun Tang

Authors
  1. Jin Wang
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  2. Hailin Tang
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  3. Xing Li
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  4. Cailu Song
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  5. Zhenchong Xiong
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  6. Xi Wang
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  7. Xiaoming Xie
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  8. Jun Tang
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Corresponding authors

Correspondence to Jin Wang or Jun Tang.

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Wang, J., Tang, H., Li, X. et al. Is surgical axillary staging necessary in women with T1 breast cancer who are treated with breast-conserving therapy?. Cancer Commun 39, 25 (2019). https://doi.org/10.1186/s40880-019-0371-y

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Keywords

  • Surgical axillary staging
  • T1 breast cancer
  • Breast-conserving therapy
  • Surveillance, Epidemiology, and End Results

Cancer Communications

ISSN: 2523-3548

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