Abstract
Background:
In women with previously treated breast cancer, occurrence and timing of second breast cancers have implications for surveillance. The authors examined the timing of second breast cancers by primary cancer estrogen receptor (ER) status in the Breast Cancer Surveillance Consortium.
Methods:
Women who were diagnosed with American Joint Commission on Cancer stage I–III breast cancer were identified within six Breast Cancer Surveillance Consortium registries from 2000 to 2017. Characteristics collected at primary breast cancer diagnosis included demographics, ER status, and treatment. Second breast cancer events included subsequent ipsilateral or contralateral breast cancers diagnosed >6 months after primary diagnosis. The authors examined cumulative incidence and second breast cancer rates by primary cancer ER status during 1–5 versus 6–10 years after diagnosis.
Results:
At 10 years, the cumulative second breast cancer incidence was 11.8% (95% confidence interval [CI], 10.7%–13.1%) for women with ER-negative disease and 7.5% (95% CI, 7.0%–8.0%) for those with ER-positive disease. Women with ER-negative cancer had higher second breast cancer rates than those with ER-positive cancer during the first 5 years of follow-up (16.0 per 1000 person-years [PY]; 95% CI, 14.2–17.9 per 1000 PY; vs. 7.8 per 1000 PY; 95% CI, 7.3–8.4 per 1000 PY, respectively). After 5 years, second breast cancer rates were similar for women with ER-negative versus ER-positive breast cancer (12.1 per 1000 PY; 95% CI, 9.9–14.7; vs. 9.3 per 1000 PY; 95% CI, 8.4–10.3 per 1000 PY, respectively).
Conclusions:
ER-negative primary breast cancers are associated with a higher risk of second breast cancers than ER-positive cancers during the first 5 years after diagnosis. Further study is needed to examine the potential benefit of more intensive surveillance targeting these women in the early postdiagnosis period.
Keywords: breast cancer, estrogen receptor, recurrence, surveillance, survivorship
INTRODUCTION
Although most women diagnosed with breast cancer are treated with curative intent, breast cancer survivors remain at risk for second breast cancer events. Surveillance imaging is an important component of posttreatment care for breast cancer survivors to facilitate early detection of second cancer events. Current guidelines from the American Society of Clinical Oncologists,1 the National Comprehensive Cancer Network,2 and the American College of Radiology3 recommend annual surveillance mammography for women with a personal history of breast cancer. However, the use of surveillance imaging in clinical practice varies by providers and facilities, and mammography at more frequent intervals is common, particularly in the first 5 years after treatment completion.4–7 Women with a personal history of breast cancer also frequently undergo breast magnetic resonance imaging (MRI) for more intensive surveillance,5,8,9 although guidelines across professional societies are variable and generally acknowledge the paucity of evidence regarding which breast cancer survivors are best served by MRI surveillance.1,2,10,11
Optimally, imaging surveillance protocols should be informed by the magnitude and timing of risk of second breast cancer events relative to the primary breast cancer diagnosis. The temporal variation in second breast cancer risk may vary by the estrogen receptor (ER) status of the primary breast cancer, which is known to predict distinct patterns of distant breast cancer recurrence and death. Prior studies have demonstrated that distant recurrence occurs earlier in women with ER-negative cancer (within the first 5 years after diagnosis) and later in women with ER-positive cancer (after the first 5 years).12–18 However, potential differences in timing of second breast cancers detectable by surveillance breast imaging for women with ER-positive versus ER-negative cancers have not been described. To better inform surveillance guidelines, we examined annual rates and cumulative incidence of second breast cancers by ER status of the primary breast cancer in a cohort of women within the Breast Cancer Surveillance Consortium (BCSC).
MATERIALS AND METHODS
Study setting
Data were collected prospectively from six BCSC registries (Carolina Mammography Registry, New Hampshire Mammography Network, San Francisco Mammography Registry, Kaiser Permanente Washington Registry, Vermont Breast Cancer Surveillance System, and Metropolitan Chicago Breast Cancer Registry).19 Registries collected information from participating imaging facilities on patient demographics, risk factors, and breast imaging examinations. Linkages were made to state or regional cancer registries and pathology and biopsy databases for breast cancer diagnoses and to state death data.
Each BCSC registry and the Statistical Coordinating Center (SCC) received institutional review board approval for all study procedures, including passive permission processes (three registries) or a waiver of consent (three registries and the SCC), to enroll participants, link data, and perform analytic studies. All procedures are Health Insurance Portability and Accountability Act-compliant. All registries and the SCC have received a Federal Certificate of Confidentiality and other protections for the identities of women, physicians, and facilities.
Study population
The study cohort included women aged 18 years and older with unilateral, American Joint Committee on Cancer (AJCC) (eighth edition),20 stage I–III primary breast cancer diagnosed in 2000–2017 who had imaging performed at a BCSC facility in the peridiagnostic period (defined as 2 years before primary diagnosis through 6 months after diagnosis) and underwent definitive surgical treatment (breast-conserving surgery [BCS] or mastectomy). We excluded women treated with bilateral mastectomy because they are not recommended to receive surveillance mammography. The following exclusions were applied based on the primary breast cancer: <6 months of follow-up after primary diagnosis (n = 1456), missing ER status (n = 941), and/or missing radiation treatment information if a woman had BCS (n = 57). We also excluded women whose initial posttreatment imaging was performed at a facility with incomplete pathology data capture (n = 5967).
Woman and primary cancer characteristics
Primary cancer characteristics and treatment were obtained from cancer registry and pathology data, including AJCC anatomic stage, tumor size (T1, ≤20 mm; T2/T3, >20 mm), tumor grade, ER status, human epidermal growth factor receptor 2 (HER2) status, type of primary surgery (BCS or mastectomy) and radiation therapy receipt, adjuvant endocrine therapy, and/or adjuvant chemotherapy. Other data collected at the time of primary cancer diagnosis included age, self-reported race and ethnicity, menopausal status, and first-degree family history of breast cancer.
Second breast cancers
Second breast cancer diagnoses, type (invasive vs. ductal carcinoma in situ), and laterality were ascertained from cancer registry data (for new primary breast cancers) and pathology data (for in-breast local recurrences and new primary breast cancers) using the earliest diagnosis >6 months after the primary cancer diagnosis. Because our primary outcome was second breast cancers detectable by surveillance imaging, mastectomy-side local recurrences were not included because surveillance imaging is not typically performed on the ipsilateral breast after mastectomy. All women were followed from primary breast cancer diagnosis for 10 years unless one of the following occurred earlier: second breast cancer diagnosis, mastectomy-side second cancer, death, last known alive date, disenrollment from health plan (one registry), or 5 years after a woman’s last imaging examination performed at a BCSC facility.
Statistical analysis
We compared the cumulative incidence of all second breast cancer events in women with ER-positive versus ER-negative primary cancers accounting for competing risks (death, mastectomy-side recurrence) and censoring at all other follow-up events. Rates of second breast cancers in years 1–5 and years 6–10 after primary breast cancer diagnosis were calculated as the number of second cancer events per 1000 person-years (1000 PY) with 95% confidence intervals (CIs) assuming a Poisson distribution based on the exact method because of small numbers of events during some intervals. We also calculated cumulative incidence and annual rates for ipsilateral second cancers and contralateral second cancers.
To explore how other primary cancer characteristics may affect second cancer risks, we also performed stratified analyses by early (stage I–IIA) versus advanced (stage IIB–III) primary cancer and treatment received (BCS without radiation therapy, BCS with radiation therapy, and mastectomy). In a secondary analysis in the subset of women with known HER2 status, we examined cumulative second cancer incidence stratified by both ER and HER2 status (primary cancer diagnosis in 2010 and later for three registries, 2007 and later for one registry, and 2001 and later for two registries). All analyses were performed using SAS (version 9.4; SAS Institute Inc.).
RESULTS
We identified 36,165 women who were diagnosed with AJCC stage I–III unilateral breast cancer in 2000–2017 at a BCSC imaging facility. After applying exclusions, the final study population consisted of 27,744 women (see Figure S1).
At primary breast cancer diagnosis, most women were aged 55 years or older (58% of ER-negative women, 68% of ER-positive women) and were non-Hispanic White (70% of ER-negative women, 80% of ER-positive women); non-Hispanic Black women comprised 17% of ER-negative breast cancers and 8% of ER-positive breast cancers. Most women were diagnosed with early stage (I–IIA) disease (75% of ER-negative women, 82% of ER-positive women) and T1 breast cancer (53% of ER-negative women, 68% of ER-positive women; Table 1) and received BCS with or without radiation (67% of ER-negative women, 73% of ER-positive women). The median follow-up was 5.7 years (interquartile range, 2.9–8.9 years).
TABLE 1.
Characteristics of 27,744 women and their primary cancers at the time of diagnosis by estrogen receptor (ER) status of the primary cancer.
| ER-positive (N = 23,139) |
ER-negative (N = 4,605) |
|||
|---|---|---|---|---|
| No. | Col % | No. | Col % | |
|
| ||||
| Age at diagnosis, years | ||||
| <40 | 790 | 3% | 336 | 7% |
| 40–54 | 6582 | 28% | 1597 | 35% |
| 55–74 | 2149 | 51% | 11,894 | 47% |
| ≥75 | 523 | 17% | 3873 | 11% |
| Year of diagnosis | ||||
| 2000–2004 | 5429 | 23% | 1217 | 26% |
| 2005–2009 | 7751 | 34% | 1823 | 40% |
| 2010–2014 | 7682 | 33% | 1238 | 27% |
| 2015–2017 | 2277 | 10% | 327 | 7% |
| Race/ethnicity (missing, n = 10) | ||||
| Asian/Pacific Islander, non-Hispanic | 1720 | 7% | 366 | 8% |
| Black, non-Hispanic | 1865 | 8% | 805 | 17% |
| Hispanic | 805 | 3% | 167 | 4% |
| Native American or American Indian, non-Hispanic | 34 | 0% | 7 | 0% |
| White, non-Hispanic | 18,505 | 80% | 3208 | 70% |
| Other/multiracial, non-Hispanic | 50 | 1% | 202 | 1% |
| AJCC anatomic stage, version 8 | ||||
| I | 13,950 | 60% | 2085 | 45% |
| IIA | 5156 | 22% | 1386 | 30% |
| IIB | 2241 | 10% | 609 | 13% |
| III | 1792 | 8% | 525 | 11% |
| Tumor size (missing, n = 313) | ||||
| T1 (<20 mm) | 15,725 | 69% | 2430 | 53% |
| T2/T3 (≥20 mm) | 7165 | 31% | 2111 | 46% |
| Tumor grade (missing, n = 722) | ||||
| Grade 1 | 6906 | 31% | 144 | 3% |
| Grade 2 | 10,831 | 48% | 810 | 18% |
| Grade 3 | 4837 | 21% | 3494 | 79% |
| Primary surgery | ||||
| BCS with radiation | 13,750 | 59% | 2367 | 51% |
| BCS without radiation | 3260 | 14% | 754 | 16% |
| Mastectomy | 6129 | 26% | 1484 | 32% |
| Adjuvant therapy (missing, n = 2154) | ||||
| Chemotherapy only | 1895 | 9% | 2891 | 67% |
| Endocrine therapy only | 10,055 | 47% | 97 | 2% |
| Both | 4789 | 23% | 207 | 5% |
| Neither | 4512 | 21% | 1144 | 26% |
| HER2 status (missing, n = 690)a | ||||
| HER2-positive | 1665 | 11% | 722 | 28% |
| HER2-negative | 12,971 | 89% | 1859 | 72% |
Abbreviations: AJCC, American Joint Commission on Cancer; BCS, breast-conserving surgery; Col, column.
Restricted to women who were diagnosed in the years after HER2 status was collected by registries (starting in 2001 for two registries, in 2007 for one registry, and in 2010 for three registries).
Cumulative second cancer incidence by ER status
Throughout the follow-up period, women with ER-negative primary breast cancers had a higher cumulative incidence of second breast cancer events than women with ER-positive breast cancers (Figure 1). The cumulative incidence at 5 years was 7.1% (95% CI, 6.3%–7.9%) and 3.6% (95% CI, 3.4%–3.9%) in women with ER-negative and ER-positive breast cancer, respectively; and, at 10 years, the cumulative incidence was 11.8% (95% CI, 10.7%–13.1%) and 7.5% (95% CI, 7.0%–8.0%) in women with ER-negative and ER-positive breast cancer, respectively.
FIGURE 1.
Cumulative risk of second breast cancers by estrogen receptor status of the primary breast cancer by time since breast cancer diagnosis. Estimated risks are depicted by solid lines, with shaded regions indicating 95% confidence intervals.
Early versus late second cancers by ER status
During the first 5 years of follow-up, women with ER-negative breast cancer had higher rates of second cancers (16.0 per 1000 PY; 95% CI, 14.2–17.9 per 1000 PY) than women with ER-positive breast cancer (7.8 per 1000 PY; 95% CI, 7.3–8.4 per 1000 PY; Table 2, Figure 2). In years 6–10, second cancer rates were similar for women with ER-negative cancer (12.1 per 1000 PY; 95% CI 9.9–14.7 per 1000 PY) and those with ER-positive cancer (9.3 per 1000 PY; 95% CI, 8.4–10.3 per 1000 PY). This pattern persisted when evaluating ipsilateral and contralateral second cancers separately, with higher ipsilateral and contralateral second cancer rates for women with ER-negative cancer during years 1–5 and similar rates for those with ER-negative and ER-positive cancers during years 6–10 (Table 2, Figure 3). During years 1–5, women with ER-negative cancer had higher rates of ipsilateral second cancers than contralateral second cancers, whereas women with ER-positive cancer had similar rates of ipsilateral versus contralateral second cancers. In all women, most ipsilateral and contralateral second breast cancers were invasive.
TABLE 2.
Second breast cancer rates (and 95% Confidence Intervals) by primary cancer ER status during early (years 1–5) versus late (years 6–10) years after primary breast cancer diagnosis.
| Years 1–5 after breast cancer diagnosis | Years 6–10 after breast cancer diagnosis | |||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
|
|
|
|||||||||||
| ER-positive | ER-negative | Total | ER-positive | ER-negative | Total | |||||||
|
|
|
|
|
|
|
|||||||
| No. of second cancers | Rate/1000 PY | No. of second cancers | Rate/1000 PY | No. of second cancers | Rate/1000 PY | No. of second cancers | Rate/1000 PY | No. of second cancers | Rate/1000 PY | No. of second cancers | Rate/1000 PY | |
|
| ||||||||||||
| All events | 716 | 7.8 (7.3–8.4) | 291 | 16.0 (14.2–17.9) | 1007 | 9.2 (8.6 −9.8) | 386 | 9.3 (8.4–10.3) | 103 | 12.1 (9.9–14.7) | 489 | 9.8 (9.0–10.7) |
| Ipsilateral | 341 | 3.7 (3.3–4.2) | 158 | 8.7 (7.4–10.1) | 499 | 4.6 (4.2–5.0) | 165 | 4.0 (3.4–4.7) | 41 | 4.8 (3.5–6.6) | 206 | 4.1 (3.6–4.7) |
| Invasive | 286 | 3.1 (2.8–3.5) | 129 | 7.1 (5.9–8.4) | 415 | 3.8 (3.4–4.2) | 142 | 3.4 (2.9–4.0) | 34 | 4.0 (2.8–5.6) | 176 | 3.5 (3.0–4.1) |
| In situ | 55 | 0.6 (0.5–0.8) | 29 | 1.6 (1.1–2.3) | 84 | 0.8 (0.6–0.9) | 23 | 0.6 (0.4–0.8) | 7 | 0.8 (0.3–1.7) | 30 | 0.6 (0.4–0.9) |
| Contralateral | 348 | 3.8 (3.4–4.2) | 111 | 6.1 (5.0–7.3) | 459 | 4.2 (3.8–4.6) | 214 | 5.2 (4.5–5.9) | 61 | 7.2 (5.5–9.2) | 275 | 5.5 (4.9–6.2) |
| Invasive | 255 | 2.8 (2.5–3.2) | 93 | 5.1 (4.1–6.3) | 348 | 3.2 (2.9–3.5) | 170 | 4.1 (3.5–4.8) | 51 | 6.0 (4.5–7.9) | 221 | 4.4 (3.9–5.1) |
| In situ | 93 | 1.0 (0.8–1.2) | 18 | 1.0 (0.6–1.6) | 111 | 1.0 (0.8–1.2) | 44 | 1.1 (0.8–1.4) | 10 | 1.2 (0.6–2.2) | 54 | 1.1 (0.8–1.4) |
Note: Laterality unknown for 57 second cancers (34 ER-positive, 23 ER-negative).
Abbreviations: ER, estrogen receptor; PY, person-years.
FIGURE 2.
Annual rates of second breast cancers by estrogen receptor status of primary cancer, per 1000 person-years. Estimated rates are depicted by solid lines, with shaded regions indicating 95% confidence intervals (CI).
FIGURE 3.
Annual rates of second ipsilateral and contralateral breast cancers by estrogen receptor status of the primary breast cancer, per 1000 person-years. Estimated rates are depicted by solid lines, with shaded regions indicating 95% confidence intervals (CI).
Secondary analyses
Differences in second cancer risks between ER-negative and ER-positive women were less pronounced among women with advanced primary cancer versus early stage primary cancer (Figure 4). For women with advanced primary cancers, cumulative risks of death from breast cancer were the most frequently observed outcome over the 10-year follow-up period (16.2% [95% CI, 13.8%–18.7%] for women with ER-negative cancers and 13.9% [95% CI, 12.5%–15.4%] for women with ER-positive cancers), exceeding cumulative second breast cancer risks (10.4% [95% CI, 8.3%–12.7%] for women with ER-negative cancers and 7.5% [95% CI, 6.5%–8.7%] for women with ER-positive cancers).
FIGURE 4.
Cumulative risk of second breast cancer by primary cancer estrogen receptor status and stage. Advanced stage, American Joint Committee on Cancer (AJCC) stage IIB–III; early stage, AJCC stage I–IIA; ER, estrogen receptor.
Women with ER-negative cancers had higher second cancer risks than women with ER-positive cancers across all treatment groups, including women who underwent BCS without radiation, BCS with radiation, and mastectomy (see Figure S1). The majority of second breast cancers had ER status concordant with that of primary breast cancers. Among second breast cancers with available ER status, 82% of ER-positive primary breast cancers and 53% of ER-negative primary breast cancers had the same ER status in subsequent second breast cancers (see Table S1).
Differences in second cancer risks by ER status were observed in women with HER2-negative primary cancers, but not in those with HER2-positive primary cancers (see Figure S3). Second breast cancer 10-year cumulative incidence was 8.0% (95% CI, 6.1%–10.4%) in ER-positive/HER2-positive women, 7.9% (95% CI, 7.1%–8.7%) in ER-positive/HER2-negative women, 10.5% (95% CI, 7.5%–14.2%) in ER-negative/HER2-positive women, and 12.4% (95% CI, 10.3%–14.7%) in ER-negative/HER2-negative women.
DISCUSSION
In this analysis of second breast cancer risk among women with a personal history of breast cancer in the BCSC, ER status of the primary invasive cancer was an important prognostic factor for both the magnitude and the timing of second breast cancer events. Overall, women who had ER-negative primary cancers had higher risks of second breast cancers, whether ipsilateral or contralateral, in the initial 5 years after diagnosis compared with women who had ER-positive breast cancers. Risks of second breast cancers were similar for women with ER-negative and ER-positive primary cancer after 5 years.
This pattern has been similarly observed in studies of regional and distant breast cancer recurrences, which tend to occur early in follow-up of women with a history of ER-negative cancers.11–15 The reasons for these differences in the timing of breast cancer events are not fully understood. Endocrine therapy used in the treatment of ER-positive disease has been shown to have a carryover effect, reducing breast cancer recurrence and mortality well after treatment cessation.17 It has also been posited that ER-positive cancer cells may have the ability to survive in a period of dormancy followed by later reactivation.21 Regardless of the etiology, these findings suggest that ER status may be an important factor to consider for decision making regarding the intensity and timing of surveillance imaging in women with a personal history of invasive breast cancer.
Our study also suggests that other characteristics of the primary breast cancer may be helpful in more precisely identifying women with ER-negative breast cancer at higher risk for second cancers during the early posttreatment period. ER-negative primary cancer was associated with higher second cancer risks among women with HER2-negative primary cancers, but not HER2-positive primary cancers, although the number of women with HER2-positive cancers in our cohort was small. Studies with larger cohorts of women who have HER2-positive cancers are needed to corroborate these findings. We also found that differences in second breast cancer risks between women with ER-negative and ER-positive disease were more pronounced in women with early stage primary cancers. For women with advanced stage at diagnosis, the competing risk of breast cancer mortality was much higher than the risk of second breast cancer.
Taken together, our findings suggest that ER status may be an important prognostic factor for identifying the women at highest risk for second breast cancer events and has not been specifically considered in surveillance guidelines to date. Recommendations for supplemental imaging in women with a personal history of breast cancer currently vary across professional societies. For example, whereas the American College of Radiology currently recommends MRI surveillance for breast cancer survivors who are diagnosed at a younger age (younger than 50 years) or who have dense breasts,10 the American Cancer Society and the National Comprehensive Cancer Network highlight the uncertainty regarding which women are most likely to benefit from surveillance imaging.1,2 Of note, among the women receiving surveillance mammography in the BCSC, approximately 25% were diagnosed before age 50 years, 39% had dense breasts at surveillance mammography,22 and 62% of these women had one or both of these characteristics.11 In contrast, only 17% of women in our cohort had ER-negative primary cancer at diagnosis. Therefore, tailoring surveillance to primary cancer ER status would target a relatively selective subpopulation of breast cancer survivors for supplemental surveillance imaging at the highest risk for second breast cancer events. Of note, although our study demonstrates that women with ER-negative cancer are at higher risk, prospective trials of imaging surveillance specifically targeting this population are not available; therefore, the clinical impact of more intensive surveillance has yet to be established. Further study is needed to evaluate whether women with ER-negative primary cancers may potentially benefit from more intensive surveillance in the early postdiagnosis period.
Strengths of this study include our large cohort of breast cancer survivors across six geographically diverse BCSC breast imaging registries with cancer diagnosis information available through state and regional cancer registries and local pathology and biopsy databases, which allowed comprehensive ascertainment of recurrent inbreast events that are typically excluded from studies that rely on cancer registries only. Our study also has limitations. Our cancer capture is limited to the geographic regions of the BCSC facilities, and cancer capture could be incomplete for women who relocated or received care outside the BCSC during the study period. Although we censored women after 5 years without surveillance imaging performed at a BCSC facility, it is possible that our results underestimated second breast cancer risk. Information regarding the presence of pathogenic variants in cancer susceptibility genes (such as BRCA1 and BRCA2) was also not available. Although rare in the overall population, these variants are more common among women with ER-negative breast cancers and thus could be an unmeasured confounder. In addition, we limited our evaluation of second events to in-breast events and did not include mastectomy-side recurrences. We chose to exclude these events because surveillance mammography is not typically performed on the ipsilateral breast after mastectomy; therefore, these risks are not informative for surveillance mammography guidelines. However, as a result, our findings may have slightly underestimated total second cancer events for women treated with mastectomy. We also are unable to distinguish between local recurrences versus ipsilateral second primary breast cancers in our data. However, this distinction may be less important for the purposes of guiding surveillance imaging, which is intended to detect both local recurrences and new cancers. Finally, despite our large cohort size, our sample size decreased as women were lost to follow-up, and our risk estimates were less precise in the later surveillance periods. Further work is needed to examine longer term rates of second cancer events in data sets of women with a personal history of breast cancer, given that the risk of distant recurrence has been shown to persist well beyond 10 years, especially for women with ER-positive primary cancers.23
In summary, women with ER-negative primary cancers are at higher risk of second breast cancer events than women with ER-positive primary cancers during the first 5 years after breast cancer treatment. Our findings suggest that primary breast cancer ER status could be used to identify women at highest risk of second breast cancer events during the early posttreatment period and should be a consideration for guidelines and decision making regarding surveillance imaging regimens for breast cancer survivors.
Supplementary Material
ACKNOWLEDGMENTS
The authors thank the participating women, mammography facilities, and radiologists for the data they have provided for this study. You can learn more about the BCSC at: http://www.bcsc-research.org/. This research was funded by the National Cancer Institute (P01CA154292, R50CA211115). Data collection for this work was additionally supported in part by funding from the National Cancer Institute (U54CA163303), the Patient-Centered Outcomes Research Institute (PCS-1504-30370), and the Agency for Health Research and Quality (R01 HS018366-01A1). The collection of cancer and vital status data used in this study was supported in part by several state public health departments and cancer registries throughout the United States. For a full description of these sources, please see: https://www.bcsc-research.org/about/work-acknowledgement. All statements in this report, including its findings and conclusions, are solely those of the authors and do not necessarily represent the views of the Patient-Centered Outcomes Research Institute, its Board of Governors or Methodology Committee, nor those of the National Cancer Institute, the National Institutes of Health, or the Agency for Health Research and Quality.
Funding information
Patient-Centered Outcomes Research Institute, Grant/Award Number: PCS-1504-30370; National Cancer Institute, Grant/Award Numbers: P01CA154292, R50CA211115, U54CA163303; Agency for Healthcare Research and Quality, Grant/Award Number: R01 HS018366-01A1
Kathryn P. Lowry reports grants from the American Cancer Society and personal fees from the Radiological Society of North America outside the submitted work. Rebecca Hubbard reports grants from Merck, the National Institutes of Health, and Pfizer Canada, Inc.; and personal fees from Johnson & Johnson Medical Devices & Diagnostics Group-Latin America, LLC, outside the submitted work. Diana S. M. Buist reports payment for participation in review activities from Women Informed to Screen Depending on Measures of Risk Data Safety and Monitoring Board outside the submitted work. Karla Kerlikowske is an unpaid consultant to Grail for the STRIVE study. Jennifer M. Specht reports grants from AbbVie, Cascadian Therapeutics, Celcuity Inc., Genentech, Merck, Pfizer, and Seattle Genetics; personal fees from Daichi Sankyo, GE Healthcare, GSKGlaxoSmithKline, Sensei Biotherapeutics, and Volastra; and travel support from A2 Biotherapeutics outside the submitted work. Janie M. Lee reports grants from GE Healthcare outside the submitted work.
Footnotes
CONFLICTS OF INTEREST STATEMENT
The remaining authors made no disclosures.
SUPPORTING INFORMATION
Additional supporting information can be found online in the Supporting Information section at the end of this article.
REFERENCES
- 1.Runowicz CD, Leach CR, Henry NL, et al. American Cancer Society/American Society of Clinical Oncology Breast Cancer Survivorship Care Guideline. J Clin Oncol. 2016;34(6):611–635. PubMed PMID: 26644543. doi:1200/JCO.2015.64.3809 [DOI] [PubMed] [Google Scholar]
- 2.National Comprehensive Cancer Network (NCCN). NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines): Breast Cancer, Version 5.2020. NCCN; 2020. Accessed July 21, 2020. https://www.nccn.org/professionals/physician_gls/pdf/breast.pdf [Google Scholar]
- 3.Lewin AA, Moy L, et al. ACR Appropriateness Criteria® stage I breast cancer: initial workup and surveillance for local recurrence and distant metastases in asymptomatic women. J Am Coll Radiol. 2019;16(11S):S428–S439. Epub 2019/11/07PubMed PMID:31685110. doi:1016/j.jacr.2019.05.024 [DOI] [PubMed] [Google Scholar]
- 4.Buist DSM, Ichikawa L, Wernli KJ, et al. Facility variability in examination indication among women with prior breast cancer: implications and the need for standardization. J Am Coll Radiol. 2020;17(6):755–764. Epub 2020/02/01PubMed PMID: 32004483; PubMed Central PMCID: PMCPMC7275918. doi:1016/j.jacr.2019. 12.020 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Henderson LM, Ichikawa L, Buist DSM, et al. Patterns of breast imaging use among women with a personal history of breast cancer. J Gen Intern Med. 2019;34(10):2098–2106. Epub 2019/08/15PubMed PMID: 31410813; PubMed Central PMCID: PMCPMC 6816668. doi:1007/s11606-019-05181-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Nguyen DL, Oluyemi E, Myers KS, Panigrahi B, Mullen LA, Ambinder EB. Variability of mammographic imaging surveillance in breast cancer survivors. J Am Coll Radiol. 2021;19(1):20–23. doi:1016/j.jacr.2021.09.040 [DOI] [PubMed] [Google Scholar]
- 7.Patel BK, Lee CS, Kosiorek HE, Newell MS, Pizzitola VJ, D’Orsi CJ. Variability of postsurgical imaging surveillance of breast cancer patients: a nationwide survey study. AJR Am J Roentgenol. 2018;210(1): 222–227. Epub 2017/10/25PubMed PMID: 29064749. doi:2214/AJR.17.17923 [DOI] [PubMed] [Google Scholar]
- 8.Stout NK, Nekhlyudov L, Li L, et al. Rapid increase in breast magnetic resonance imaging use: trends from 2000 to 2011. JAMA Intern Med. 2014;174(1):114–121. Epub 2013/11/20PubMed PMID: 24247482; PubMed Central PMCID: PMCPMC4145846. doi:1001/jamaintern med.2013.11958 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Wernli KJ, DeMartini WB, Ichikawa L, et al. Patterns of breast magnetic resonance imaging use in community practice. JAMA Intern Med. 2014;174(1):125–132. Epub 2013/11/20PubMed PMID: 24247555; PubMed Central PMCID: PMCPMC3905972. doi:1001/jamainternmed.2013.11963 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Monticciolo DL, Newell MS, Moy L, Niell B, Monsees B, Sickles EA. Breast cancer screening in women at higher-than-average risk: recommendations from the ACR. J Am Coll Radiol. 2018;15(3 pt A):408–414. Epub 2018/01/27PubMed PMID: 29371086. doi:1016/j.jacr.2017.11.034 [DOI] [PubMed] [Google Scholar]
- 11.Lawson MB, Herschorn SD, Sprague BL, et al. Imaging surveillance options for individuals with a personal history of breast cancer: AJR expert panel narrative review. AJR Am J Roentgenol. 2022;219(6): 854–868. Epub 2022/05/12PubMed PMID: 35544374. doi:2214/AJR.22.27635 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Colleoni M, Sun Z, Price KN, et al. Annual hazard rates of recurrence for breast cancer during 24 years of follow-up: results from the International Breast Cancer Study Group Trials I to V. J Clin Oncol. 2016;34(9):927–935. Epub 2016/01/21PubMed PMID: 26786933; PubMed Central PMCID: PMCPMC4933127. doi:1200/JCO.2015. 62.3504 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Hess KR, Pusztai L, Buzdar AU, Hortobagyi GN. Estrogen receptors and distinct patterns of breast cancer relapse. Breast Cancer Res Treat. 2003;78(1):105–118. Epub 2003/03/04. PubMed PMID: 12611463. doi:1023/a:1022166517963 [DOI] [PubMed] [Google Scholar]
- 14.Jatoi I, Bandos H, Jeong JH, et al. Time-varying effects of breast cancer adjuvant systemic therapy. J Natl Cancer Inst. 2016;108(1): djv304. Epub 2015/11/01PubMed PMID: 26518884; PubMed Central PMCID: PMCPMC4635647. doi:1093/jnci/djv304 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Pagani O, Price KN, Gelber RD, et al. Patterns of recurrence of early breast cancer according to estrogen receptor status: a therapeutic target for a quarter of a century. Breast Cancer Res Treat. 2009;117(2):319–324. Epub 2009/01/13PubMed PMID: 19137426; PubMed Central PMCID: PMCPMC3589101. doi:1007/s10549-008-0282-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Saphner T, Tormey DC, Gray R. Annual hazard rates of recurrence for breast cancer after primary therapy. J Clin Oncol. 1996;14(10): 2738–2746. Epub 1996/10/01PubMed PMID: 8874335. doi:1200/JCO.1996.14.10.2738 [DOI] [PubMed] [Google Scholar]
- 17.Early Breast Cancer Trialists’ Collaborative Group, Davies C, Godwin J, et al. Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: patient-level meta-analysis of randomised trials. Lancet. 2011;378(9793):771–784. Epub 2011/08/02PubMed PMID: 21802721; PubMed Central PMCID: PMCPMC3163848. doi:1016/S0140-6736(11)60993-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Early Breast Cancer Trialists’ Collaborative Group, Peto R, Davies C, 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(9814): 432–444. Epub 2011/12/14PubMed PMID: 22152853; PubMed Central PMCID: PMCPMC3273723. doi:1016/S0140-6736(11) 61625-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Breast Cancer Surveillance Consortium. Research Sites and Principal Investigators. Accessed February 10, 2022. https://www.bcsc-research.org/about/sites
- 20.American Joint Committee on Cancer. AJCC Cancer Staging Manual. 8th ed. Springer International Publishing; 2017. [Google Scholar]
- 21.Zhang XH, Giuliano M, Trivedi MV, Schiff R, Osborne CK. Metastasis dormancy in estrogen receptor-positive breast cancer. Clin Cancer Res. 2013;19(23):6389–6397. Epub 2013/12/04PubMed PMID: 24298069; PubMed Central PMCID: PMCPMC3878717. doi:1158/1078-0432.CCR-13-0838 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Lee JM, Ichikawa LE, Wernli KJ, et al. Digital mammography and breast tomosynthesis performance in women with a personal history of breast cancer, 2007-2016. Radiology. 2021;300(2):290–300. Epub 2021/05/19PubMed PMID: 34003059; PubMed Central PMCID: PMCPMC8328154. doi:1148/radiol.2021204581 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Pan H, Gray R, Braybrooke J, et al. 20-Year risks of breast-cancer recurrence after stopping endocrine therapy at 5 years. N Engl J Med. 2017;377(19):1836–1846. Epub 2017/11/09PubMed PMID: 29117498; PubMed Central PMCID: PMCPMC5734609. doi:1056/NEJMoa1701830 [DOI] [PMC free article] [PubMed] [Google Scholar]
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