Abstract
Background
Population-based breast screening programs diagnose cancers at earlier stage when they are easier to treat. Indeed, individuals screened as part of the Ontario Breast Screening Program (OBSP) are diagnosed with a lower stage of breast cancer than those who have never been screened. We sought to determine if adherence to OBSP guidelines is associated with differences in the rate of death from breast cancer in addition to cancer stage at diagnosis.
Methods
48,927 women ≥ 51 years diagnosed with a first primary breast cancer in Ontario 2010–2017 were included and classified as an adherent screener, partial screener, or non-screener. The cohort was developed using administrative health databases linked by Ontario Health. Cause-specific hazard ratios (HR) and 95% confidence intervals (CI) were used to examine the association between adherence to OBSP guidelines and the rate of breast cancer death adjusting for age, rurality, and history of a prior cancer diagnosis. Death from non-breast cancer causes was considered a competing risk.
Results
Compared to adherent screenings, non-screeners and non-adherent screeners had higher rates of death from breast cancer (HR: 3.59, 95% CI 3.30–3.90 and HR: 1.69, 95% CI 1.47–1.95 respectively). Further, non-adherent screeners (i.e., screened ≥ once) had a lower rate of breast cancer death than non-screeners (HR: 0.47, 95% CI 0.41–0.54).
Interpretation
Individuals screened in the OBSP have a lower rate of death from breast cancer than non-screeners, even if they are not meeting screening guidelines. These findings suggest women should be encouraged to participate in breast screening regardless of their frequency of use.
Supplementary Information
The online version contains supplementary material available at 10.1007/s10549-025-07754-y.
Keywords: Breast cancer, Screening, Mortality
Introduction
Breast cancer is the most commonly diagnosed cancer in women worldwide [1, 2], and one in eight Canadian women will develop the disease in their lifetime [3]. Breast cancer-related mortality has been on the decline since the 1980 s [4] This can be attributed to advancements in adjuvant treatments (e.g., targeted therapies like tamoxifen, aromatase inhibitors and trastuzamab) [5], and the implementation of population-based screening programs [4, 6]. Screening with mammography diagnoses cancers at an earlier stage when they are easier to treat, leading to better outcomes.
Provincial breast cancer screening programs have existed in Canada since 1988 [7]. In Ontario, individuals ages 50 to 74 years who are not at high risk of breast cancer [8], are eligible to be screened with mammography every two years as part of the Ontario Breast Screening Program (OBSP), with annual screening available for women with extremely dense breasts or a strong family history [9] (note: the OBSP expanded screening guidelines to include individuals in their forties in October 2024). We previously showed that individuals who are screened according to OBSP guidelines are more likely to be diagnosed with a lower stage of breast cancer than those who attend screening less frequently or have never been screened [10].
The objective of this study is to examine if adherence to OBSP screening guidelines is associated with lower rates of death from breast cancer. While many clinical trials have shown a clear benefit of mammography on breast cancer-specific survival [11–13], results have not always been consistent [14, 15]. Understanding the impact of adherence to screening guidelines on rates of breast cancer death outside the context of the highly constrained conditions of a clinical trial are less understood.
Methods
Study design, setting and population
This study is a retrospective, population-based cohort study of individuals diagnosed with breast cancer in Ontario, Canada from 2010 to 2017. This cohort has been described previously [10]. Briefly, we included all women ages 51–74 years diagnosed with a first primary breast cancer of any stage and histology who were eligible for screening in the OBSP (N = 49,769). We only included women 51 to 74 years of age to reflect those eligible for the average risk OBSP during the period of follow-up. People aged 30 to 69 who are eligible for, or enrolled in the High Risk OBSP (N = 842) were excluded. This resulted in 48,927 individuals included in our analysis.
Data sources
Ontario Health demographic and administrative databases were used for the current study. Age, cancer-related and cause of death variables were obtained from the Ontario Cancer Registry (OCR). Date and primary cause of death are available in the OCR from death certificate information collected by the Ontario Register General. Primary cause of death using ICD-10 codes were used to categorize cause of death as breast cancer (i.e., ICD-10 C50) or other causes. Individuals without a death entry were considered alive at end of follow-up (December 31 st, 2019). History of prior non-breast cancers was obtained from the OCR and categorized as yes/no.
Screening information was obtained from the Integrated Cancer Management System (ICMS) database, which contains data collected by the OBSP including information on screening episodes and their outcomes. The OBSP started in 1990, and each year performs approximately 700,000 screening mammograms across the province. Screening behavior was categorized as ‘adherent’, ‘non-adherent’ or ‘no screening’ based on our previous work [10]. Screening episodes that were diagnostic (i.e., symptomatic) were not considered in the classification of screening behaviors. Non-screeners had no record in the ICMS database, indicating that they had not had a mammogram prior to their breast cancer diagnosis. While guidelines recommend biannual screening, we classified participants as adherent screeners if they had a mammogram at least once every three years from age 50 for biannual recall, and once every two years following annual recall (e.g., individuals with dense breasts or family history) to allow for scheduling delays. Non-adherent screeners had at least one record in the ICMS but did not qualify as adherent screeners.
Rurality, income and other demographic variables were extracted from the Postal Code OM Conversion File Plus (PCCF+). Rurality was categorized according to Statistics Canada’s definition of a census metropolitan area (CMA) to represent four different urban groups as sizes ranging from < 100.000 people to over 1,500,000 people. Individuals who did not live within a CMA were classified as rural. Participants without information on population density were classified as missing (N = 743, 1.5%).
Statistical analysis
Cumulative incidence function curves stratified by adherence to OBSP guidelines were produced with death from other causes treated as a competing risk, and formally compared using Gray’s test. Cause-specific regression analysis was used to examine the association between screening behavior and breast cancer death adjusting for age at diagnosis, rurality, and prior history of non-breast cancer. Death from non-breast cancer-related death was treated as a competing risk. Time was assessed from diagnosis until death, or end of follow-up (December 31st, 2019). Stage at diagnosis was not adjusted for as it is along the causal pathway between our exposure (i.e., screening behavior) and outcome (i.e., breast cancer-specific death).
Sensitivity analyses restricting to individuals diagnosed with invasive breast cancer (i.e., excluding individuals with DCIS, N = 4,852) and/or index by 6 months to assess the impacts of length and lead time bias, respectively.
A p value less than 0.05 was considered statistically significant and all tests were two-sided. All analyses were conducted using SAS v9.4.
Ethical approval
Research Ethics Board approval was received from the University of Toronto (#37488). Participant consent was not sought as data were provided by a prescribed entity under Ontario’s privacy legislation (Ontario Health) which can collect, use, and provide access to routinely collected health information for research.
Results
Characteristics for our sample have been previously described, [10] and can be found in Table 1. The median age at breast cancer diagnosis was 63 years (interquartile range (IQR): 57–68), and 7.8% (N = 3,829) had a history of a prior non-breast cancer diagnosis. Women were most commonly diagnosed with stage I breast cancer (40.0%, N = 19,587), and less than 4% were diagnosed at stage IV (3.8%, N = 1851). Approximately half of women were classified as adherent screeners (53.4%, N = 26,108), and about a third as non-screeners (33.3%, N = 16,273).
Table 1.
Demographic variables and breast cancer characteristics stratified by screening behavior for women diagnosed with a first breast cancer in Ontario between 2010 and 2017
| Overall | Adherent screeners | Non-adherent screeners | Non-screeners | |
|---|---|---|---|---|
| (N = 48,927) | (N = 26,108) | (N = 6546) | (N = 16,273) | |
| Agea | ||||
| Median (IQR) | 63 (57–68) | 63 (57–68) | 64 (59–69) | 62 (55–68) |
| Neighborhood income | ||||
| Highest | 10,459 (21.4%) | 5802 (22.2%) | 1367 (20.9%) | 3290 (20.2%) |
| Middleb | 28,944 (59.2%) | 15,740 (60.3%) | 3789 (57.9%) | 9415 (57.9%) |
| Lowest | 8781 (18.0%) | 4226 (16.2%) | 1265 (19.3%) | 3290 (20.2%) |
| Unknown | 743 (1.5%) | 340 (1.3%) | 125 (1.9%) | 278 (1.7%) |
| Urban/rural community sizec | ||||
| Urban population < 100,000 | 4437 (9.1%) | 2447 (9.4%) | 557 (8.5%) | 1433 (8.8%) |
| Urban population 100,000–499,999 | 10,998 (22.5%) | 6520 (25.0%) | 1561 (23.9%) | 2917 (17.9%) |
| Urban population 500,000–1,499,999 | 8046 (16.4%) | 4151 (15.9%) | 971 (14.8%) | 2924 (18.0%) |
| Urban population > 1,500,000 | 18,806 (38.4%) | 9302 (35.6%) | 2581 (39.4%) | 6923 (42.5%) |
| Rural area | 5897 (12.1%) | 3348 (12.8%) | 751 (11.5%) | 1798 (11.1%) |
| Unknown | 743 (1.5%) | 340 (1.3%) | 125 (1.9%) | 278 (1.7%) |
| Prior non-breast cancer | ||||
| No | 45,098 (92.2%) | 24,058 (92.2%) | 5991 (91.5%) | 15,049 (92.5%) |
| Yes | 3829 (7.8%) | 2050 (7.9%) | 555 (8.5%) | 1244 (7.5%) |
| Cancer stage | ||||
| I | 19,587 (40.0%) | 12,016 (46.0%) | 2705 (41.3%) | 4866 (29.9%) |
| II | 14,163 (29.0%) | 6830 (26.2%) | 1966 (30.0%) | 5367 (33.0%) |
| III | 4726 (9.7%) | 1875 (7.2%) | 555 (8.5%) | 2296 (14.1%) |
| IV | 1851 (3.8%) | 365 (1.4%) | 190 (2.9%) | 1296 (8.0%) |
| DCIS | 4852 (9.9%) | 3053 (11.7%) | 641 (9.8%) | 1158 (7.1%) |
| Not stagedd | 183 (0.4%) | 97 (0.4%) | 30 (0.5%) | 56 (0.3%) |
| Unknown | 3565 (7.3%) | 1872 (7.2%) | 459 (7.0%) | 1234 (7.6%) |
| Follow-up time (years) | ||||
| Mean (range) | 3.6 (> 0–8.0) | 3.7 (> 0.0–8.0) | 2.7 (> 0.0–8.0) | 3.9 (> 0.0–8.0) |
| Outcome measures | ||||
| Breast cancer-specific death | 2869 (5.9) | 804 (3.1) | 261 (4.0) | 1804 (11.1) |
| Death from causes other than breast | 1483 (3.0) | 618 (2.4) | 167 (2.6) | 698 (4.3) |
IQR interquartile range, DCIS ductal carcinoma in situ
aData presented here (except outcome measures) have previously been presented in our prior manuscript[10]
aAge for this cohort was restricted to participants between the age of 51 and 74 to reflect those eligible for the Ontario Breast Cancer Screening Program average risk eligibility group
bThe middle income classification represents a combination of all individuals who fell within the middle three quintiles of the neighborhood income distribution named lower-middle, middle, upper-middle income
cCommunity size is differentiated by population size. Urban area is defined as being part of a population center, while rural areas are areas surrounding urban areas without a population center
dNon-staged breast cancer represents invasive stage zero forms of breast cancer such as Paget's disease, Phyllodes tumors, and angiosarcoma of the breast
The median length of follow-up was 3.6 years (range: > 0 to 8 years) from the time of breast cancer diagnosis. Over the follow-up period, 5.9% (N = 2,869) died of breast cancer, and 3.0% (N = 1483) died from causes other than breast cancer. Cumulative incidence function curves comparing breast cancer-specific mortality based on adherence to the OBSP breast cancer screening times is present in Fig. 1. There was evidence of a significant difference in the cumulative incidence of breast cancer-specific mortality based on adherence to OBSP breast cancer screening guidelines (Gray’s p value < 0.0001). Adherent screeners had the lowest cumulative incidence of breast cancer-specific mortality, and non-screeners had the highest breast cancer-specific mortality.
Fig. 1.
Cumulative incidence functions for breast cancer specific mortality stratified by breast cancer screening adherence
The relationship between screening behavior and death from breast cancer are presented in Table 2. Compared to non-screening women, adherent (HR: 0.28, 95% CI: 0.26–0.30) and non-adherent-screeners (HR: 0.47, 95% CI 0.41–0.54) had a statistically significant lower rate of death from breast cancer. Conversely, non-adherent screeners had a significantly higher rate of breast cancer-specific mortality than adherent screeners (HR: 1.69, 95% CI 1.47–1.95). Similar findings were observed when individuals diagnosed with DCIS were excluded from the sample and/or when index was set to 6 months later (See Supplementary Table 1).
Table 2.
Cause-specific hazard ratios (HR) and 95% confidence intervals (CI) for the relationship between screening behaviors and death from breast cancer in Ontario (2010–2017)
| Death from breast cancer HR (95% CI)a |
|
|---|---|
| Screening behaviorb | |
| Non-adherent versus adherent | 1.69 (1.47–1.95) |
| Non-screening versus adherent | 3.59 (3.30–3.90) |
| Adherent versus non-screening | 0.28 (0.26–0.30) |
| Non-adherent versus non-screening | 0.47 (0.41–0.54) |
| Age (per 5 years) | 1.07 (1.04–1.10) |
| Urban/rural community size | |
| Urban Area 1,500,000 + people | Ref |
| Urban 500,000–1,499,999 | 1.27 (1.14–1.41) |
| Urban 100,000–499,999 | 1.41 (1.28–1.56) |
| Urban < 100,000 | 1.38 (1.21–1.58) |
| Rural | 1.41 (1.25–1.59) |
| Unknown | 3.32 (2.70–4.08) |
| Prior non-breast cancer | |
| No | Ref |
| Yes | 0.94 (0.81–1.08) |
HR Cause-specific hazard ratio, 95% CI 95% confidence interval, Ref reference
aEstimates adjusted for age at breast cancer diagnosis, urban/rural community size, and history of prior diagnosis of invasive non-breast cancer (yes/no)
bScreening behavior was defined as follows: adherent screeners were screened by OBSP every three years for biannual recall and every two years for annual recall; non-adherent screeners
Interpretation
We previously found that in Ontario, individuals who are not screened have an almost nine times higher odds of being diagnosed with stage IV disease than those who screened according to OBSP guidelines [10]. Findings from the current study extend on this work showing that individuals who were screened according to OBSP guidelines (i.e., adherent screeners) had a substantially lower rate of death from breast cancer than non-screeners. Further, the benefits of participating in the screening program were not limited to women who met screening guidelines. Women who had at least one mammogram but did not meet OBSP guidelines also had a substantially lower rate of death from breast cancer than non-screeners. This shows that even some screening can benefit individuals with respect to earlier stage at diagnosis [10] and lower rates of breast cancer-specific death. Thus, women who are eligible for the OBSP should be encouraged to attend even if they do not attend as frequently as recommended by the OBSP guidelines (i.e., some screening is better than no screening).
Breast cancer mortality is declining, and early detection by breast cancer screening programs is a contributing factor to these lower rates [4, 6]. We previously reported adherence to OBSP guidelines is inversely associated with stage of breast cancer at diagnosis [10]. Non-adherent screeners were diagnosed with a lower stage of breast cancer than non-screeners, but not as low of a stage as adherent screeners. Prior randomized control trials and observational studies have compared breast cancer mortality outcomes among women who underwent breast cancer screening [16–21], and most have observed positive results. Randomized control trials from Sweden [21] and New York [19] have found significant reductions in breast cancer-specific mortality among women randomized to receive breast cancer screening compared to the non-screening group. Further, a follow-up study was conducted from a randomized breast cancer screening study in Sweden just among participants who developed breast cancer [20]. Both our study, and this follow-up study [20] observed a significantly lower breast cancer-specific mortality rate among breast cancer survivors who are screened for breast cancer than non-screeners. Our study further stratified screeners into those who met breast cancer screening guidelines and those that were screened less frequently, and we found that women who adhered to a breast screening program had the lowest rate of breast cancer mortality compared to those who were non-adherent and non-screeners. This suggests that breast cancer screening is associated with a lower rate of breast cancer death in addition to a lower stage of breast cancer at diagnosis.
Breast cancer screening guidelines typically recommend that women 50 to 74 years of age receive biannual mammograms, although recent changes to guidelines now recommend screening individuals starting at age 40 [13, 22, 23] The OBSP has extended the eligibility age for starting screening to 40 in October 2024 [24] At this time of this study, individuals ages 50 to 74 years of age who are not at high risk of breast cancer could have a mammogram every one (for annual recall) to two years (for standard recall). Individuals with extremely dense breasts or a strong family history are offered annual mammograms. While these mammograms come with no cost to the individual and do not require a physician referral, still just over half of women diagnosed with breast cancer in Ontario from 2010 to 2017 attended the OBSP in accordance with breast cancer screening guidelines. This means that thousands of individuals in Ontario who are eligible for screening are not currently participating.
The reasons why individuals may not be screened according to OBSP guidelines are complex and multi-factorial [25, 26]. These factors may be structural (e.g., access to an OBSP screening site or knowledge of the OBSP program), or personal (e.g., they do not want to participate or do not feel there is a benefit to participating). Further, screening for breast cancer is not without potential harms, including the potential for overdiagnosis [27] and false-positives leading to unnecessary biopsies and the associated anxiety [16]. In the current study, we observed that women who are screened at least once but do not meet OBSP guidelines (i.e., non-adherent screeners) still experience some benefits from this screening. While non-adherent screeners had a higher rate of breast cancer mortality than adherent screeners, non-adherent screeners did experience a significantly lower rate of breast cancer death than non-screeners.
This study has several limitations that need to be considered. First, information on mammograms conducted outside of the OBSP is not available in our dataset meaning women classified as non-screeners may have undergone breast screening elsewhere. If present, this misclassification error would bias our results towards the null. Second, breast cancer treatments are associated with stage at breast cancer diagnosis and are known to significantly impact patient outcomes. While treatment would be along the causal pathway between breast cancer diagnosis and breast cancer death, statistically accounting for the impact of different treatments on this association could help explain why adherent and non-adherent screeners experienced a lower rate of breast cancer death. While some treatment information was available, treatment information needed to test this hypothesis was not.
Individuals self-select to enroll in the OBSP, and individuals who choose to participate in the OBSP or adhere to the OBSP guidelines may have certain characteristics that lower their risk of dying from breast cancer independent of the impacts of breast cancer screening. To assess for the potential impact of this selection bias, we corrected our HRs comparing breast cancer-specific mortality between adherent screeners and non-screeners using the method proposed by Duffy et al. [28]. While our HR was attenuated (from 0.29 to 0.40), our results still indicate a significantly lower rate of breast cancer mortality among adherent screeners compared to non-screeners. In addition, our results may be affected by lead time bias from screening detecting cancer at lower stages which take more years to result in death, and length bias as a result of in situ tumors being more commonly identified among women who participate in the OBSP than those who do not. We assessed the impact of these biases by excluding women diagnosed with ductal carcinoma in situ, and excluding women with less than 6 months follow-up time (see Supplementary Table 1). While the effect estimates were attenuated compared to our primary analyses, these effect estimates were still demonstrated a significantly lower breast cancer-specific mortality rate in adherent and non-adherent screeners compared to non-screeners.
In conclusion, we observed that among women diagnosed for breast cancer, those who were screened according to OBSP guidelines had a lower rate of breast cancer-specific mortality than those who did not. In addition, even sporadic screening was associated with a lower rate of breast cancer-specific mortality than never attending. Overall, this suggests that some screening is better than no screening and that individuals eligible for screening should be encouraged to participate, even if they are not able to attend as frequently as recommended by local guidelines. This could change the way screening programs engage with reluctant screeners to increase overall participation rates and improve long-term outcomes.
Supplementary Information
Below is the link to the electronic supplementary material.
Author contributions
GMA and JDB conceived of the design of the study, oversaw analysis and drafting the manuscript. RAGC contributed to the study design and conducted the data analysis and drafted of the manuscript. AA contributed to the data analysis. All authors have read and approved the final manuscript.
Funding
This study was supported by the Canadian Institutes of Health Research (CIHR) Catalyst Grant: 322718 (GMA). Rebecca A. G. Christensen was supported by a CIHR Fellowship Award: 473057 and a CIHR grant RN312225-376411 (JDB).
Data availability
Data from Ontario Health is available to researchers upon reasonable request.
Declarations
Competing interests
Parts of this material are based on data and information provided by Ontario Health (Cancer Care Ontario) [and includes data received by Ontario Health (Cancer Care Ontario) from the Canadian Institute for Health Information (CIHI)]. The opinions, reviews, views, and conclusions reported in this publication are those of the authors and do not necessarily reflect those of Ontario Health (Cancer Care Ontario) [CIHI]. No endorsement by Ontario Health (Cancer Care Ontario) [CIHI] is intended or should be inferred. The authors have no conflict of interests to report.
Footnotes
Publisher's Note
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Associated Data
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Supplementary Materials
Data Availability Statement
Data from Ontario Health is available to researchers upon reasonable request.