De-Implementation of Low-Value Care for Women 70 Years of Age or Older with Low-Risk Breast Cancer During the COVID-19 Pandemic

This study demonstrated significant de-implementation of adjuvant radiotherapy among women 70 years of age or older with ER+, HER2–, cN0, T1 IBC after the start of the COVID-19 pandemic in 2020. Among these patients with low-risk breast cancer, adjuvant radiotherapy is associated with a small reduction in locoregional recurrence, but no survival benefit.^6,8 Among patients eligible for omission of post-BCS radiotherapy, the probability of radiotherapy receipt decreased by approximately one third from 2020–2022 to 2012–2019.

Although the retrospective nature of this study did not allow for the direct determination of a causal relationship between the COVID-19 pandemic and radiotherapy utilization, the abrupt de-implementation of adjuvant radiotherapy among eligible patients in 2020 supports an effect from the COVID-19 pandemic rather than more generalized efforts at de-escalation of breast cancer treatment. Specifically, resource limitations during the acute phase of the pandemic increased awareness about the benefits of avoiding low-value care. This was supported by the April 2020 COVID-19 Pandemic Breast Cancer Consortium expert consensus, which explicitly recommended omission or deferral of radiotherapy for patients 65 to 70 years of age or older with early-stage ER+ IBC.¹⁶ Before 2020, the rates of radiotherapy in this study remained stable despite several opportunities for de-implementation during the last decade, including release of 10-year data from CALGB 9343 in 2013, inclusion of low-value breast cancer care as a focus of the Choosing Wisely campaign in 2016, and release of the results from PRIME II in 2017.

In contrast to the de-escalation of adjuvant radiotherapy among the patients with low-risk breast cancer, there was no change in rates of radiotherapy delivery to patients who were not candidates for omission during the study period. Although the COVID-19 pandemic in 2020 complicated the delivery of radiotherapy, the study institution was able to provide continued high rates of radiotherapy to patients with high-risk breast cancer who required adjuvant treatment. These practice patterns, with targeted de-implementation of radiotherapy for patients with low-risk breast cancer and simultaneous high rates of radiotherapy for patients with high-risk breast cancer, persisted for at least 2 years after the acute phase of the pandemic without rebound to pre-pandemic patterns. This suggests sustained changes in clinical practice patterns and provider comfort with not recommending radiotherapy for patients at low risk for locoregional recurrence.

Although the rates of SLNB among the patients in the low-risk cohort decreased significantly from 2012 to 2022, this trend predated 2020 and did not appear to have been affected by the COVID-19 pandemic. Additionally, the rates of SLNB among the patients in the high-risk cohort also decreased during the study period, although to a lesser extent. This finding likely was related to several factors. First, this study restricted eligibility for SLNB omission to patients with T1 tumors in order to define a low-risk cohort eligible for both radiotherapy and SLNB omission. However, SSO and Choosing Wisely both recommend SLNB omission for patients with “early-stage cancer,” which can be interpreted by providers to include larger tumors.

Second, the decision to perform SLNB is based on clinical stage. In circumstances in which SLNB is initially omitted, providers may not elect to return to the operating room for axillary staging if a tumor was upstaged on final pathology.

Finally, in 2016, the study institution piloted a clinical trial evaluating the safety and efficacy of SLNB omission for patients 65 years of age or older with ER+, HER2–, T1-T2 IBC. The patients with T2 tumors in this trial for whom SLNB was omitted would have been classified as part of the high-risk cohort who were ineligible for SLNB omission in the current study.

The finding that radiotherapy and SLNB utilization were affected differently by the COVID-19 pandemic likely reflects discrepancies in provider attitudes on the potential harms of these two services. Although radiotherapy requires significant utilization of health care resources and risks exposure of both patients and providers to COVID-19 infection, performing SLNB at the time of a planned breast cancer operation may appear relatively benign to surgeons. This distinction is also reflected in the April 2020 recommendations by the COVID-19 Pandemic Breast Cancer Consortium. Whereas there is specific guidance to omit or defer radiotherapy for patients 65 to 70 years of age or older with early-stage ER+ IBC, there is no recommendation to avoid axillary staging for this patient population.¹⁶ Prior qualitative research evaluating provider barriers to de-implementation of low-value SLNB demonstrated that surgeons view SLNB as an easy and low-risk procedure.¹⁷ However, despite this bias, SLNB is not benign. Rates of lymphedema after SLNB are approximately 5%, and studies have shown that patients who receive axillary staging are significantly more likely to receive adjuvant radiotherapy despite their potential as appropriate candidates for omission of both low-value therapies.^18,19 This was supported by the current study, which found that the patients in the low-risk cohort who received SLNB, even if found to have tumor-free lymph nodes, were significantly more likely to receive adjuvant radiotherapy. The cascade effect, in which one low-value procedure leads to increased utilization of other low-value therapies, is a described phenomenon that exists across medical subspecialities and has been shown to result in significant harm to patients, health care costs, and emotional distress.^20,21

Predictably, the factors associated with increased odds of SLNB and radiotherapy utilization among the patients in the low-risk cohort included younger age, larger tumors, high-grade tumors, and tumor-involved lymph nodes. The finding that grade 3 disease was significantly associated with receipt of radiotherapy among patients otherwise candidates for omission is interesting because it reflects a general concern among radiation oncologists that patients with grade 3 tumors were underrepresented in CALGB 9343 and PRIME II.²² In the findings of CALGB 9343, tumor grade was not reported, and only 3% of the patients in PRIME II had grade 3 tumors. This discrepancy likely was due in part to the overall low-risk biology of small ER+ breast cancers in women 70 years of age or older. Only 13% of the patients in this study who were eligible for radiotherapy omission had grade 3 disease compared with 41% of the patients who were not eligible for omission. However, high-grade disease is known to be one of the strongest independent risk factors for locoregional recurrence, and among these patients, radiotherapy administration is associated with substantial reductions in recurrence risk.²³ Thus, radiotherapy for patients with grade 3 tumors may be beneficial even for older patients with early-stage, ER+/HER2– disease.

The finding that nodal involvement is significantly associated with increased rates of radiotherapy is frequently cited as a reason not to de-escalate SLNB, because the nodal status may have an impact on what adjuvant therapies a patient receives.²⁴ However, in the modern era of molecular testing, the importance of pathologic staging has diminished. The RxPonder trial demonstrated that the benefit of chemotherapy for post-menopausal women with ER+ IBC depends on tumor biology, and thus the Oncotype Dx score rather than the identification of nodal metastases now largely dictates whether a patient receives chemotherapy.²⁵ The potential benefit of adjuvant radiotherapy for women 70 years of age or older with ER+/HER2– IBC who have tumor-involved lymph nodes is of greater debate. However, it is worth noting that although two thirds of the patients in CALGB 9343 did not receive nodal staging, the 10-year locoregional recurrence rate was lower than 10%, and the rate of axillary recurrence was only 3% for the women who omitted radiotherapy and were treated with endocrine therapy alone.⁶ This finding is further supported by data from retrospective studies that have found no difference in survival rates among patients 70 years of age or older with ER+, HER2–, cN0 IBC regardless of radiotherapy receipt if endocrine therapy is administered, even among patients with nodal metastases on SLNB.²⁶

Finally, the rates of nodal positivity are low among patients meeting the criteria for omission of axillary staging. In the low-risk cohort, 11% of the patients had sentinel lymph node involvement compared with 35% of the patients in the cohort that was not eligible for omission of axillary staging. This is supported by other studies that have found the rate of nodal involvement among women 70 years of age or older with cN0, T1, ER+/HER2– IBC to be lower than 10%.²⁷

The target rate for SLNB and radiotherapy de-implementation among patients eligible for omission of these therapies is unknown. However, the dramatic decrease in rates of completion ALND among patients with one or two tumors involving lymph nodes who received BCS and radiotherapy after dissemination of the ACOSOG Z0011 trial can serve as a model for successful de-implementation.²⁸ National data suggest that among patients meeting eligibility criteria for Z0011, the rates of completion ALND decreased from 63% in 2004 to 14% in 2016, a relative reduction of 78%.¹³ Thus, despite the significant de-implementation of radiotherapy and SLNB among women 70 years of age or older with low-risk ER+ IBC observed in the current study, opportunity likely exists for continued de-escalation.

Prior work has shown that several factors are associated with utilization of low-value SLNB and radiotherapy for breast cancer patients. First, patient age is strongly correlated with SLNB and radiotherapy receipt among patients who are candidates for omission.^12,29 This is supported by findings in the current study showing that few patients older than 80 years with low-risk ER+ IBC received SLNB or radiotherapy.

Second, both patients and providers refer to the importance of considering physiologic age in addition to biologic age when age-based guidelines are evaluated. Qualitative work has shown that patients who feel healthier than average are more likely to desire aggressive care despite recommendations for omission.³⁰ Similarly, surgeons frequently describe making treatment decisions based on a patient’s functional status rather than a patient’s biologic age.¹⁷ However, despite the bias that healthy patients with low-risk ER+ IBC might benefit more from SLNB and radiotherapy, it is important to note that the patients included in CALGB 9343 had a higher overall survival than age-matched women in the general population, suggesting that the results of this trial apply equally to women who are healthier than average and without significant comorbid conditions.⁶

Finally, patient desire to pursue more versus less medical care may be an inherent personal trait. This concept has been shown through the medical maximizer-minimizer scale, in which “medical maximizers“ tend to elect for health care interventions in situations in which it may not be necessary, whereas “medical minimizers” tend to avoid health care inventions unless they are absolutely necessary.³¹ The correlation between medical maximizer-minimizer preferences and receipt of SLNB and radiotherapy among women with low-risk breast cancer has previously been shown.^32,33 The tendency for medical maximizers to want “everything done” may explain, at least in part, why patients with low-risk IBC who received SLNB were more likely to receive radiotherapy even in the absence of nodal positivity.

This study was limited by its single-institution nature, so these findings may not be representative of national practice patterns. However, post-pandemic data from national databases such as the National Cancer Database (NCDB) and the Surveillance, Epidemiology, and End Results (SEER) program will not be available for analysis for several years. Additionally, due to the contemporary nature of this study, there are no long-term data on whether patients for whom radiotherapy was omitted completed their recommended course of adjuvant endocrine therapy. However, the decision to omit radiotherapy is based on clinical judgment as to whether a patient is likely to tolerate adjuvant endocrine therapy, so evaluating initiation of endocrine therapy is likely an appropriate surrogate.

Patient age and tumor characteristics alone do not capture the nuances involved in the decision for a patient to omit or receive axillary staging and radiotherapy. The decision relies on shared decision-making regarding the potential risks versus the benefits of these therapies, and not every patient who has been identified in the low-risk cohort may be truly appropriate for omission of radiotherapy and SLNB.

Finally, factors other than the COVID-19 pandemic may have affected the trends observed in this study. However, the sharp change in radiotherapy practice patterns in 2020 with little to no change in the years before suggests a strong correlation with the COVID-19 pandemic.

In conclusion, this study demonstrated appropriate de-escalation of adjuvant radiotherapy for women 70 years of age or older with cN0, T1, ER+, HER2– IBC during the COVID-19 pandemic without a change in rates of radiotherapy receipt among patients with high-risk breast cancer. This reflects intentional, evidence-based change in provider practice patterns to avoid low-value care, which has been sustained over time. Although there has been de-implementation of SLNB for patients eligible for omission of axillary staging since 2012, this trend appears to predate 2020 and did not change with the COVID-19 pandemic. This demonstrates that reduction in low-value care offers an opportunity for dissemination of strategies to reduce overtreatment at other institutions and at a national level.