Abstract
In the past two decades, three prospective randomized trials demonstrated that elderly women with early-stage hormone positive breast cancer had equivalent disease-specific mortality regardless of axillary surgery. In 2016, the Choosing Wisely campaign encouraged patients and providers to reconsider the role of axillary surgery in this population. We sought to identify factors that contribute to adopting non-operative management of the axilla in these patients.
We performed a retrospective analysis of women ≥70 years old with cT1/T2, hormone positive invasive ductal carcinoma who underwent partial or total mastectomy, with/without axillary from the National Cancer Database from 2004–2015. We used multivariable log-binomial regression to model the risk of undergoing axillary surgery across region, care setting, and Charlson-Deyo scores, and analyzed temporal trends using Poisson regression.
From 2004–2015, 87,342 of 99,940 women who met inclusion criteria (83%) had axillary surgery. Over time, axillary surgery increased from 78% to 88% (p<0.001). This rise was consistent across region (p=0.81) and care setting (p=0.09), but flattened as age increased (p<0.001). Omitting axillary surgery was more likely in patients treated in New England (RR 0.88, 95% CI 0.86, 0.89) and patients ≥85 (RR 0.66, 95% CI 0.65, 0.67).
Axillary surgery continues to be the preferred option of axillary management in elderly women with early stage, clinically node negative, hormone-positive, invasive breast cancer despite no survival benefit. Identifying factors to improve patient selection and dissemination of current recommendations can improve adoption of current evidence on axillary surgery in the elderly.
Introduction
In the past two decades, advances in axillary management of early stage breast cancer has allowed the de-escalation of surgical interventions, most notably fewer axillary lymph node dissections (1, 2). These studies have allowed us to improve the quality of life in breast cancer survivors and decrease the morbidity associated with axillary lymphadenectomy. As the population in the United States ages over the next two decades, there is an expected rise in cancer incidence in the elderly with patients ≥65 years old accounting for 70% of all cancer cases diagnosed by 2030 (3). Historically, this population has been under-represented in clinical trials. Three prospective randomized trials in the United States and Europe demonstrated that in elderly women with early stage estrogen receptor (ER)/progesterone receptor (PR) positive breast cancer, there was equivalent disease-specific mortality regardless of axillary lymph node sampling and dissection (4–7). Despite this evidence, the incidence of axillary surgery within the past decade remained high despite the findings of these studies (8–12).
Partnering with the American Board of Internal Medicine (ABIM), the Society of Surgical Oncology (SSO) launched the Choosing Wisely campaign in 2016 to facilitate the shared-decision making process between patients and physicians. Their first recommendation was against the routine use of sentinel lymph node biopsy in early stage, clinically node negative, hormone-positive breast cancer in women ≥70 years old (13).
The goal of this study was to determine longitudinal trends of axillary surgery in elderly women with clinically node-negative hormone positive breast cancer. We hypothesized that with increasing level I evidence supporting omission of axillary surgery, we would see a decrease in the use of axillary surgery mirroring the level of evidence supported in the literature. A secondary aim of the study was to determine the impact of chronological age, comorbidities and geographic location on axillary surgery use in this population.
Methods
Data source
A cohort of clinically early stage, hormone-positive breast cancer patients was constructed using the National Cancer Database (NCDB) site-specific participant use file (PUF). The NCDB is a national, hospital-based cancer registry program jointly implemented by the Commission on Cancer of the American College of Surgeons and the American Cancer Society. The NCDB collects detailed tumor information, patient characteristics, primary treatment and outcome data from over 1,500 commission-accredited cancer programs, which treat over 70% of all incident cancers in the United States. Though a lack of important patient attributes such as weight and smoking status can be problematic for some outcome studies, the NCDB is a particularly strong data source for understanding care patterns stratified by baseline patient characteristics (14).
Study population
Our study cohort was designed to address the target population of the Choosing Wisely Campaign. We included women ≥70 years old diagnosed with a clinical T1 or T2, ER positive and PR positive, infiltrating duct carcinoma between 2004 and 2015. HER2 receptor status was a new variable introduced in the NCDB in 2012. To control for HER2 positive disease in patients prior to 2012, we excluded patients who received systemic chemotherapy. Additionally, to control for heterogeneity among histology, we limited our study to patients with invasive ductal carcinoma. Patients underwent partial or total mastectomy with or without axillary surgery. We defined axillary surgery as sentinel lymph node biopsy (SLNB) with or without axillary lymph node dissection (ALND). Additionally, women with missing information on chemotherapy or surgical axillary management were excluded.
Statistical analysis
Descriptive statistics were used to assess patient demographics, facility characteristics, and treatment plans across patient age (categorized as 70–74, 75–79, 80–84, and ≥85 years old). Comorbidities were captured using the Charlson-Deyo Score provided by the PUF, which is categorized as 0, 1, 2, and ≥3. Facility type was assigned by the Commission on Cancer Accreditation and included community cancer program, comprehensive community cancer program, academic/research program, and integrated network cancer program. US Census division and region were also captured in the PUF and analyzed.
Potential linear trends in axillary surgery use between 2004 and 2015 were assessed using Poisson regression. Age-, comorbidity score-, facility type-, and region-stratified trends were also assessed using similar methods. Differences in trends over time by categories within stratifying variables were assessed using interaction terms and Wald chi-square tests. Multivariable log-binomial regression was used to model the odds of receiving axillary surgery across age group, Charlson-Deyo Score, facility type and region, after adjustment for all variables of interest and year of diagnosis, race, area-level income, area-level education, and primary insurance type. Due to low prevalence, uninsured women were excluded from multivariable modeling (n=294). The results of the Poisson model guided the decision to control for time in the model but exclude stratum-time interactions since there were significant trends but no significant difference in trends (i.e. trend lines were parallel).
Results
From 2004–2015, we identified 113,130 women who met our initial inclusion criteria. We excluded 13,049 patients that received systemic chemotherapy and an additional 141 patients due to unknown axillary surgery status. Summary of patient demographics, stratified by age, is in Table 1. Of the 99,940 women who met final inclusion criteria, 90% of the patients were Caucasian, 6% African American and 5% Hispanic. The majority of patients resided in metropolitan areas (82%) and were treated at a comprehensive cancer program (52%). Twenty-five percent of patients were treated at an academic center. The majority of patients were insured (98%) through either federal programs (Medicare/Medicaid) (88%) or through private insurance (10%). Ninety-five percent of patients had a Charlson-Deyo Score of 0 or 1. When stratified by age, the majority of patients in the cohort were ages 70–74 (40%), followed by 75–79 (31%), 80–84 (19%), and 85 years or older (10%). No clinically meaningful differences among patient demographics were seen among age groups.
TABLE 1.
Patient demographics and facility characteristics among older women with early stage, hormone receptor positive breast cancer, stratified by age group.
| 70–74 | 75–79 | 80–84 | ≥85 | |
|---|---|---|---|---|
| 39,521 (40%) | 30,569 (31%) | 19,478 (19%) | 10,372 (10%) | |
| Race, n (%) | ||||
| White | 35,616 (91) | 27,776 (91) | 17,749 (92) | 9,495 (92) |
| Black | 2,485 (6) | 1,852 (6) | 1,144 (6) | 608 (6) |
| Asian | 872 (2) | 589 (2) | 357 (2) | 153 (2) |
| Other | 282 (1) | 169 (1) | 106 (1) | 48 (1) |
| Hispanic, n (%) | 1,149 (3) | 874 (3) | 464 (3) | 204 (2) |
| Median area-level incomea, n (%) | ||||
| <$38,000 | 5,555 (14) | 4,315 (14) | 2,796 (14) | 1,457 (14) |
| $38,000-$47,999 | 8,928 (23) | 7,017 (23) | 4,637 (24) | 2,427 (24) |
| $48,000-$62,999 | 10,997 (28) | 8,665 (29) | 5,360 (28) | 3,023 (29) |
| >$63,000$ | 13,858 (35) | 10,401 (34) | 6,567 (34) | 3,390 (33) |
| Area-level high school graduationb, n (%) | ||||
| ≤79% | 4,908 (13) | 3,739 (12) | 2,350 (12) | 1,226 (12) |
| 79.1%−87.0% | 9,222 (23) | 7,335 (24) | 4,706 (24) | 2,433 (24) |
| 87.1%−93% | 13,870 (35) | 10,726 (35) | 6,861 (35) | 3,764 (37) |
| >93% | 11,357 (29) | 8,614 (28) | 5,449 (28.1) | 2,878 (28) |
| Residence typec, n (%) | ||||
| Metro | 32,280 (84) | 25,127 (85) | 16,184 (85) | 8,601 (85) |
| Urban | 5,520 (14) | 4,062 (14) | 2,464 (13) | 1,303 (13) |
| Rural | 685 (2) | 555 (2) | 329 (2) | 164 (2) |
| Charlson-Deyo score, n (%) | ||||
| 0 | 30,605 (77) | 23,365 (76) | 14,863 (76) | 7,959 (77) |
| 1 | 7,081 (18) | 5,696 (19) | 3,635 (19) | 1,901 (18) |
| 2 | 1,395 (4) | 1,167 (4) | 780 (4) | 385 (4) |
| ≥3 | 440 (1) | 341 (1) | 200 (1) | 127 (1) |
| Primary insurance, n (%) | ||||
| Uninsured | 144 (<1) | 97 (<1) | 32 (<1) | 21 (0.2) |
| Private insurance | 4,985 (12.8) | 2,981 (9.9) | 1,645 (8.5) | 792 (7.7) |
| Medicaid/Medicare/Other Gov. | 33,968 (86.9) | 27,193 (89.8) | 17,620 (91.3) | 9,436 (92.1) |
| Facility type, n (%) | ||||
| Community Cancer Program | 4,322 (11) | 3,572 (12) | 2,604 (13) | 1,480 (14) |
| Comprehensive Community Cancer Program | 20,405 (52) | 16,046 (53) | 10,340 (53) | 5,575 (54) |
| Academic/Research Program | 10,481 (27) | 7,605 (25) | 4,419 (23) | 2,291 (22) |
| Integrated Network Cancer Program | 4,313 (11) | 3,346 (11) | 2,115 (11) | 1,026 (10) |
| Facility location, n (%) | ||||
| New England | 2,528 (6) | 1,950 (6) | 1,355 (7) | 716 (7) |
| Middle Atlantic | 5,832 (15) | 4,728 (16) | 3,059 (16) | 1,546 (15) |
| South Atlantic | 8,504 (22) | 6,392 (21) | 3,931 (20) | 2,007 (19) |
| East North Central | 7,710 (20) | 6,094 (20) | 4,066 (21) | 2,272 (22) |
| East South Central | 2,421 (6) | 1,902 (6) | 1,128 (6) | 612 (6) |
| West North Central | 3,450 (9) | 2,750 (9) | 1,787 (9) | 962 (9) |
| West South Central | 2,243 (6) | 1,758 (6) | 1,106 (6) | 582 (6) |
| Mountain | 1,871 (5) | 1,402 (5) | 791 (4) | 377 (4) |
| Pacific | 4,962 (13) | 3,593 (12) | 2,255 (12) | 1,298 (13) |
Median household income for each patients ZIP code was reported by NCDB and estimated using the patient’s ZIP code at time of diagnosis and linking to the 2012 American Community Survey
Area-level high school graduation was estimated as the number of adults within the patient’s ZIP code who did not graduate from high school which was also captured in the 2012 American Community Survey and reported by NCDB
Residence type was determined using Federal Information Processing Standard Publication (FIPS) county code to USDA rural-urban continuum codes and reported by NCDB
Overall, the incidence of axillary surgery was 83% (n = 87,342) with a nodal positivity rate of 12% (n = 12,372). Longitudinally, we found the incidence of axillary surgery increased over from 78% in 2004 to 88% in 2015 (p <0.001, Figure 1). This increase in incidence occurred regardless of patient age (Figure 2a), Charlson-Deyo comorbidity score (Figure 2b), or Census division (Figure 2c). Additionally, the increased use of axillary surgery over time was seen across all measured socioeconomic and demographic factors including race, area-level income, area-level education, primary insurance status, and facility type (data not shown).
FIGURE 1.

Probability of undergoing axillary surgery, among older women with early stage, hormone receptor positive breast cancer.
FIGURE 2.

Probability of undergoing axillary surgery, among older women with early stage, hormone receptor positive breast cancer, stratified by A) age, B) Charlson-Deyo comorbidity score, and C) Census division.
Additional analysis was performed to determine the effect of type of operation (mastectomy compared to partial mastectomy) on the role of axillary surgery. In our cohort, 25.4% of patients (n = 25,365) underwent mastectomy, with patients older than 80 years old undergoing mastectomy more frequently than younger patients (28% patients ≥80, 24% patients < 80). Axillary surgery was equivocal between mastectomy and partial mastectomy patients, 44% and 46% respectively.
Beginning in 2012, the NCDB also collected specific detail on the type of axillary performed (sentinel lymph node biopsy or axillary lymphadenectomy). We performed a subset analysis to evaluate the type of axillary surgery performed between 2012–2015 to determine if practice changes affected the incidence of axillary surgery. From 2012–2015, the incidence of sentinel lymph node biopsies increased from 70% to 78%. This increase was statistically significant across all age groups (p < 0.0001), with the greatest increase in sentinel lymph node biopsy incidence in the 80–84 age group.
After multivariable adjustment, we found significant differences in the use of axillary surgery by age, comorbidity status and geographic census division from 2004–2015 (Table 2). Women 80–84 years old were 10% less likely and women aged ≥85 years old were almost 40% less likely to undergo axillary surgery, compared to women 70–74 years old (RR 0.87, 95% CI 0.87, 0.88 and RR 0.66, 95% CI 0.65, 0.67, respectively). Despite the differences in axillary surgery use by age, 61% of 0.66, 95% CI 0.65, 0.67, respectively). Despite the differences in axillary surgery use by age, 61% of women ≥85 years old still underwent axillary surgery. Patients with a Charlson-Deyo score of ≥2 had also had a lower incidence of axillary surgery, however the decrease in incidence compared to patients with fewer comorbidities was modest (RR 0.95, 95% CI 0.94, 0.96, p < 0.0001). Patients treated in New England were consistently less likely to receive axillary surgery (RR 0.88, 95% CI 0.86, 0.89), however the incidence of axillary surgery followed the increasing national trajectory between 2004 and 2015 (Figure 2c). We found minimal differences in axillary surgery over time across race, income level, insurance status, and facility type.
TABLE 2.
Association between age, Charlson-Deyo comorbidity score, facility type, and facility location with axillary surgery utilization among older women with early stage, hormone receptor positive breast cancer.
| Underwent axillary surgery N (%) | Crude RR (95% CI) | Adjusteda RR (95% CI) | |
|---|---|---|---|
| Age group, years | |||
| 70–74 | 37,398 (95) | REF | REF |
| 75–79 | 27,711 (91) | 0.96 (0.95, 0.96) | 0.97 (0.96, 0.97) |
| 80–84 | 15,858 (81) | 0.86 (0.85, 0.87) | 0.87 (0.87, 0.88) |
| ≥85 | 6,375 (61) | 0.65 (0.64, 0.66) | 0.66 (0.65, 0.67) |
| Charlson-Deyo score | |||
| 0 | 67,452 (88) | REF | REF |
| 1 | 15,887 (87) | 0.99 (0.98, 0.99) | 0.99 (0.98, 0.99) |
| 2 | 3,100 (83) | 0.95 (0.93, 0.96) | 0.95 (0.94, 0.97) |
| ≥3 | 903 (82) | 0.93 (0.90, 0.95) | 0.94 (0.92, 0.96) |
| Facility type | |||
| Community Cancer Program | 10,481 (88) | REF | REF |
| Comprehensive Community Cancer Program | 46,202 (88) | 1.01 (1.00, 1.02) | 1.00 (0.99, 1.00) |
| Academic/Research Program | 21,156 (85) | 0.98 (0.97, 0.98) | 0.98 (0.98, 0.99) |
| Integrated Network Cancer Program | 9,503 (88) | 1.01 (1.00, 1.02) | 0.99 (0.98, 1.00) |
| Facility location | |||
| New England | 4,875 (74) | REF | REF |
| Middle Atlantic | 12,993 (86) | 1.15 (1.13, 1.17) | 1.12 (1.11, 1.14) |
| South Atlantic | 18,631 (89) | 1.20 (1.18, 1.22) | 1.14 (1.13, 1.16) |
| East North Central | 17,406 (86) | 1.16 (1.14, 1.18) | 1.13 (1.11, 1.15) |
| East South Central | 5,344 (88) | 1.18 (1.16, 1.20) | 1.13 (1.11, 1.15) |
| West North Central | 8,135 (91) | 1.22 (1.20, 1.24) | 1.16 (1.14, 1.17) |
| West South Central | 5,241 (92) | 1.24 (1.22, 1.26) | 1.15 (1.14, 1.17) |
| Mountain | 3,988 (90) | 1.21 (1.19, 1.23) | 1.14 (1.12, 1.14) |
| Pacific | 10,729 (89) | 1.19 (1.17, 1.21) | 1.14 (1.12, 1.15) |
Abbreviations: RR, risk ratio; CI, confidence interval; REF, reference group
Adjusted for age, Charlson-Deyo score, facility type, Census division, year of diagnosis, race, area-level income, area-level education, and primary insurance type; uninsured women were excluded due to low prevalence (n=294)
Discussion
This study found that the incidence of axillary surgery remains high (83%) among women age 70 or older with hormone receptor positive T1 or T2 breast cancer. Rather than the predicted decrease of axillary surgery over time, our study found a 10% increase in receipt of axillary surgery over the last decade, and increases were seen regardless of age at diagnosis, comorbidity status, facility type, and facility location. After adjusting for these factors, women with advanced age and among women treated in New England had a lower incidence of axillary surgery, however axillary surgery performed in this patient population followed national trends and still increased over time. Our results are consistent with other studies, which have shown persistently high incidences (76%−89%) of axillary surgery in this patient population in a similar time period (8–10).
Advances in breast cancer care have allowed patients the ability de-escalate from invasive surgical approaches to minimize morbidity. In recent years, prospective trials in both Europe and the United States demonstrated equivalent survival of observation compared to axillary surgery in elderly women with early stage, hormone positive breast cancer (4–7). Several studies have reported on usage of axillary surgery in older women, with early stage ER+PR+/− breast cancers (8–10). In a national database study published in 2013, Pesce and colleagues found the incidence of axillary surgery from 2004–2010 among women 70 or older with cT1 ER/PR+ invasive breast cancer to be 89% (8). Despite evidence supporting the safety of axillary observation in this patient population, we found, consistent with others, that axillary surgery remains high. Despite the supporting evidence within the literature showing the safety of omitting axillary surgery in the elderly population, we found the incidence of axillary surgery continues to rise over time regardless of socioeconomic or demographic factors. This is the first study to assess the longitudinal impact of these prior studies on the incidence of axillary surgery over time. With additional time to disseminate the information to the treating physicians, the expected result would be fewer axillary surgeries (4–7). Our data demonstrates that this is not correct and, in fact, the number of axillary surgeries rises continually during our study period.
We also evaluated if surgical approach may influence the incidence of axillary surgery over time. In the surgical management of the breast, Plichta and colleagues performed a comprehensive analysis of breast cancer presentation and management in young and elderly patients (20). They found a decreased incidence of mastectomies in the elderly (20). Our findings of 25% of patients undergoing mastectomies were consistent with their findings. From a technical perspective, one may assume that the inclusion of a SLNB at the time of mastectomy may be less morbid and may not increase operative time significantly. We found that the incidence of axillary surgery was equivocal between mastectomy and partial mastectomy patients, suggesting additional factors may influence recommending axillary surgery in this population. The paradigm shift in the role of SLNB should not be underestimated. Over the past decade, SLNB has supplanted ALND as an acceptable and definitive approach to managing the clinically node negative axilla (1,2). Our subset analysis of available data from 2012–2015 on the type of axillary surgery performed found a significant shift from ALND towards SLNB, particularly in patients above the age of 80. With a less morbid surgical option, surgeons may be more inclined to offer SLNB rather than forgo the opportunity to surgically stage the axilla.
In older breast cancer patients, the purported rationale for routine sentinel lymph node biopsies is based on the assumption that the invasive procedure is a relatively low risk operation. Sentinel lymph node biopsy-associated morbidity is not insignificant, as lymphedema, chronic pain, and axillary web syndrome can interfere with a patient’s activities of daily living and can significantly impact quality of life, particularly in elderly patients with multiple other co-morbidities (21). A recent meta-analysis reported that patients undergoing SLNB had incidences of lymphedema as high as 8%, but more significantly the prevalence of chronic pain (15–56%), loss of strength (5–35%) and axillary web syndrome (12–20%) were not trivial (21). Despite published prospective randomized trials demonstrating no overall survival benefit to routine axillary surgery in older ER+ breast cancer patients, our findings of the increasing high axillary surgery use imply that the dissemination of the pivotal trial results has been inadequate (4–7). The sentinel node biopsy is not a trivial operation in an older patient and surgeons should continue to weigh the risks and benefits of axillary surgery, particularly in older patients with multiple co-morbidities and with advancing age.
Another justification for continued axillary surgery in these patients is that pathologic nodal status provides valuable prognostic information that is crucial in determining the appropriate adjuvant systemic therapy. In our analysis, a positive node was found in 12% of patients who underwent axillary surgery, which is consistent with previously reported findings (17). Bello and colleagues found the overall risk for pathologic node positivity in elderly women with hormone positive disease was 15% and that this was reduced in half (8%) in patients with low grade, clinically early-stage tumors (17). The prospective, randomized trials in this same low grade, early stage, elderly ER+ breast cancer population all demonstrated that the pathologic status of the axilla did not impact overall survival given that their elderly ER+ patients who all took tamoxifen (4–7). Collectively, these trials were investigating low risk Luminal A breast cancers well before the subtyping of breast cancers was described (19). As our understanding of the various heterogeneous molecular tumor phenotypes improves, the true utility of nodal status in breast cancer may be called in question as newer molecular driven studies may better predict disease progression and recurrence rather than nodal status in selected patients (11). Gene panel testing has also refined the systemic adjuvant decision-making process, particularly in node-negative hormone positive breast cancer. Current National Comprehensive Cancer Network (NCCN) guidelines recommend the use of a 21-gene RT-PCR panel to guide the decision for recommending systemic therapy in women with Stage II hormone positive invasive breast cancer (15). Perhaps the necessary investigation in the elderly ER+ breast cancer patient should be the recurrence score, not the axillary nodal status.
Our secondary analysis aimed to identify factors guiding clinical decisions to avoid axillary surgery in this population. We found advanced age did statistically decrease the likelihood a patient would undergo axillary surgery particularly in patients 85 or older. However, we found that patient age is not the only factor influencing shared decision-making in axillary surgery in the elderly. Underlying co-morbidities did seem to factor into surgical decision-making, however the difference in incidence of axillary surgery between patients with higher (2+) and lower (0–1) Carlson-Deyo scores was modest. These findings may support the perceived minimal risk of axillary surgery when discussing surgical options with patients, despite results from the meta-analysis that demonstrated the wide range of complications associated with the least invasive axillary surgery, sentinel node biopsy (21). While we found an increased axillary surgery across all patient and facility characteristics during the study period, New England facilities had persistently lower use compared to other geographic divisions in the United States. While we do not know the reasons for this trend, identifying New England as an outlier creates opportunities for future studies to identify characteristics that led to this practice variation and potentially greater adoption of axillary surgery recommendations in the elderly. As Yao points out, the surgeon has the ability to disseminate current evidence to the general population in our ability to ‘nudge’ surgical treatment options (22) and understanding regional variability in practice patterns may help identify opportunities for implementation of evidence-based practices.
This study is not without limitations. First, while the NCDB is a large national database that captures 70% of incidence cancer cases each year, its findings may not generalize to the entire United States population. Additionally, while specific breast cancer variables including the type of axillary surgery are reported, they were not accurately captured in NCDB until 2013, therefore we could not account for how the type of axillary surgery (sentinel lymph node biopsy versus axillary lymph node dissection) may affect surgical practice patterns over time. Additionally, while NCDB is the only national cancer registry that collects information on recurrence, it is currently not available to researchers due to missing data accuracy concerns (23,24). Despite these limitations, this is one of the only studies describing the longitudinal trends of real-world axillary surgery use in elderly women and an important benchmark on use before the 2016 ABIM/SSO Choosing Wisely campaign.
In conclusion, despite prospective randomized trial evidence that axillary surgery can be safely avoided in elderly breast cancer patients with early, hormone receptor positive disease, surgeons continue to perform axillary surgery in these patients at high and increasing incidence. Axillary surgery does not improve breast-cancer specific survival in elderly, hormone positive patients, and surgeons must balance patient specific co-morbidities and life expectancy with surgical risks when making decisions about patient treatment. Surgeons continue to play an important role in guiding shared decision making in axillary surgery. Future studies on the impact of the Choosing Wisely campaign, and gaining a better understanding of molecular tumor profiling and applying implementation science to disseminate current evidence should be conducted to improve shared decision-making and quality of life in elderly patients with early stage breast cancer.
Synopsis.
Despite prospective randomized trial evidence that axillary surgery can be safely avoided in elderly breast cancer patients with early, hormone receptor positive disease, surgeons continue to perform axillary surgery in these patients at high and increasing incidence.
Footnotes
All authors have no pertinent commercial or financial interests to disclose
References
- 1.Giuliano AE, Hunt KK, Ballman KV, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA. 2011. February 9;305(6):569–75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Galimberti V, Cole BF, Zurrida S, 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. April;14(4):297–305. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Smith BD, Smith GL, Hurria A, et al. Future of cancer incidence in the United States: burdens upon an aging, changing nation. J Clin Oncol. 2009. June 10;27(17):2758–65 [DOI] [PubMed] [Google Scholar]
- 4.Hughes KS, Schnaper LA, Berry D, et al. Lumpectomy plus tamoxifen with or without irradiation in women 70 years of age or older with early breast cancer. N Engl J Med. 2004. September 2;351(10):971–7. [DOI] [PubMed] [Google Scholar]
- 5.Rudenstam CM, Zahrieh D, Forbes JF, 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. January 20;24(3):337–44. [DOI] [PubMed] [Google Scholar]
- 6.Martelli G, Boracchi P, Ardoino I, 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. December;256(6):920–4. [DOI] [PubMed] [Google Scholar]
- 7.Hughes KS, Schnaper LA, Bellon JR, et al. Lumpectomy plus tamoxifen with or without irradiation in women age 70 years or older with early breast cancer: long-term follow-up of CALGB 9343. J Clin Oncol. 2013. July 1;31(19):2382–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Pesce C, Czechura T, Winchester DJ, et al. Axillary surgery among estrogen receptor positive women 70 years of age or older with clinical stage I breast cancer, 2004–2010: a report from the National Cancer Data Base. Ann Surg Oncol. 2013. October;20(10):3259–65. [DOI] [PubMed] [Google Scholar]
- 9.Chagpar AB, Hatzis C, Pusztai L, et al. Association of Lymph Node Evaluation with Survival in Women Aged 70 Years or Older With Clinically Node-Negative Hormone Receptor Positive Breast Cancer. Ann Surg Oncol. 2017;24(10):3073–3081. [DOI] [PubMed] [Google Scholar]
- 10.Tamirisa N, Thomas SM, Fayanju OM, et al. Axillary Nodal Evaluation in Elderly Breast Cancer Patients: Potential Effects on Treatment Decisions and Survival. Ann Surg Oncol. 2018;25(10):2890–2898. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Boughey JC, Haffty BG, Habermann EB, Hoskin TL, Goetz MP. Has the Time Come to Stop Surgical Staging of the Axilla for All Women Age 70 Years or Older with Hormone Receptor-Positive Breast Cancer? Ann Surg Oncol. 2017;24(3):614–617. [DOI] [PubMed] [Google Scholar]
- 12.Downs-Canner S, Zabor EC, Wind T, et al. Radiation Therapy After Breast-Conserving Surgery in Women 70 Years of Age and Older: How Wisely Do We Choose? Ann Surg Oncol. 2019;26(4):969–975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.ABIM Foundation. http://www.choosingwisely.org/societies/society-of-surgical-oncology/ July 12, 2016. Accessed May 23, 2019.
- 14.Boffa DJ, Rosen JE, Mallin K, et al. Using the National Cancer Database for Outcomes Research: A Review. JAMA Oncol. 2017. December 1;3(12):1722–1728. [DOI] [PubMed] [Google Scholar]
- 15.NCCN Clinical Practice Guidelines in Oncology – Breast Cancer version 1.2019 March 14,2019. https://www.nccn.org/professionals/physician_gls/pdf/breast.pdf Accessed May 29, 2019.
- 16.Welsh JL, Hoskin TL, Day CN, et al. Predicting Nodal Positivity in Women 70 Years of Age and Older with Hormone Receptor-Positive Breast Cancer to Aid Incorporation of a Society of Surgical Oncology Choosing Wisely Guideline into Clinical Practice. Ann Surg Oncol. 2017;24(10):2881–8. [DOI] [PubMed] [Google Scholar]
- 17.Bello DM, Russell C, McCullough D, et al. Lymph Node Status in Breast Cancer Does Not Predict Tumor Biology. Ann Surg Oncol. 2018;25(10):2884–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Ross DT, Perou CM. A comparison of gene expression signatures from breast tumors and breast tissue derived cell lines. Dis Markers. 2001;17(2):99–109 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Dominici LS, Sineshaw HM, Jemal A, et al. Patterns of axillary evaluation in older patients with breast cancer and associations with adjuvant therapy receipt. Breast Cancer Res Treat (2018) 167:555–566. [DOI] [PubMed] [Google Scholar]
- 20.Plichta JK, Thomas SM, Vernon R, et al. Breast cancer tumor histopathology, stage at presentation, and treatment in the extremes of age. Breast Cancer Res Treat (2020) 180:227–235. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Hanne Verbelen H, Gebruers N, Eeckhout F, et al. Shoulder and arm morbidity in sentinel node-negative breast cancer patients: a systematic review Breast Cancer Res Treat (2014) 144:21–31. [DOI] [PubMed] [Google Scholar]
- 22.Yao C, Boughey J. ‘Nudging’ surgeons and patients to de-escalation of surgery for breast cancer. Ann Surg Oncol (2018) 25:2777–2780. [DOI] [PubMed] [Google Scholar]
- 23.In H, Bilimoria KY, Stewart AK, et al. Cancer recurrence: an important but missing variable in national cancer registries. Ann Surg Onc (2014) 21: 1520–1529. [DOI] [PubMed] [Google Scholar]
- 24.Pezzi CM. Big data and clinical research in oncology: the good, the bad, the challenges and the opportunities. Ann Surg Oncol (2014) 21: 1506–1507. [DOI] [PubMed] [Google Scholar]
