Mammographic Breast Density, Benign Breast Disease, and Subsequent Breast Cancer Risk in 3.9 Million Korean Women

Via Peters

Summary

Women with dense breasts and benign breast disease had an elevated risk of future breast cancer and could benefit from a tailored mammography screening strategy.

Key Results

  • ■ Among 3.9 million women, breast cancer risk was 1.36% in women with fatty breast tissue (Breast Imaging Reporting and Data System [BI-RADS] density category A) and 3.2% in women with extremely dense breasts (BI-RADS density category D) over a median follow-up period of 10.6 years.

  • ■ The 10-year risk of breast cancer was 1.10% in women with benign breast disease and fatty breast tissue and 2.64% in women with benign breast disease and extremely dense breasts.

Introduction

Mammographic breast density and benign breast disease are considered strong risk factors for developing breast cancer (14). Women with dense breast tissue have a three-fold higher risk of breast cancer than do women with fatty breast tissue (1), and women with a history of benign breast disease might have up to a two-fold higher risk of breast cancer than women with no history of benign breast disease (2,3). In addition, benign breast disease and breast density were found to be significantly associated with each other (5).

Although breast density and benign breast disease are strong risk factors for breast cancer, few studies have comprehensively elucidated their combined effects (5,6). Previous studies (5,6) have suggested that the density category, as determined using the Breast Imaging Reporting and Data System (BI-RADS), and benign breast disease were independent risk factors for breast cancer, presenting stepwise increments in accordance with the presence of benign breast disease and increasing density category. However, these studies were conducted in Western populations, and to our knowledge, findings in Asian women, who have higher breast density than White women (7), remain unclear. In addition, mammographic breast cancer screening can identify the presence of benign breast disease and breast density; thus, quantification of future breast cancer risk based on mammographic screening results could provide feedback for personalized risk assessment and planning of future prevention strategies (8).

Given the higher risk of developing breast cancer among women with benign breast disease and dense breasts (5,6), differences in breast density between Asian and Western populations, and the dearth of information about risk-based screening in the Asian population, we believe that the present investigation is the largest study to examine benign breast disease and breast density in East Asian women and would help identify Asian women who could benefit from supplemental screening strategies (8,9). Thus, in this study, we investigated the risk of breast cancer associated with the combination of mammographic density and benign breast disease among women in South Korea, where population-based mammographic breast cancer screening is provided for all women aged at least 40 years.

Materials and Methods

This retrospective study was approved with a waiver of informed consent by the members of the institutional review board (approval no. HYUIRB-202106–003–1). This study used secondary data; thus, no ethical or legal concerns were raised against performing the study. The National Health Insurance Service granted permission to use the National Health Insurance Service-National Health Information Database (NHIS-NHID). Informed consent was waived because all screened populations agreed to transfer their screening results to NHIS-NHID, and the National Health Insurance Service database was constructed after the anonymization of individual identities.

Study Settings and Study Sample

This study used data from the NHIS-NHID in Korea. The National Health Insurance Service is a compulsory health insurance system that covers the entire Korean population. The NHIS-NHID includes information on demographics, health care use, vital statistics, and national health screening results of the Korean population (10). Among national health screening programs, the national breast cancer screening program provides biennial mammography screening for all women aged at least 40 years, with trained radiologists assessing the mammograms (11). This study used data from breast cancer screening results, including mammographic breast density, presence of benign breast disease based on mammograms read by radiologists (12), and data regarding other relevant factors embedded in the NHIS-NHID database.

Our initial database included women aged at least 40 years who underwent mammographic screening between January 2009 and December 2010. All participants were followed until the date of breast cancer diagnosis, date of death, or December 31, 2020, whichever came first (median follow-up, 10.6 years). If women underwent mammographic screening more than once between 2009 and 2010, then we used data from the first screening. We excluded participants who had a history of any type of cancer before the date of mammographic screening, participants with missing information on breast density and benign breast disease information, or those whose mammographic findings were suspicious for breast cancer (BI-RADS categories 4 or 5) or were incomplete (BI-RADS categories 0 and 3). Participants whose age at screening was less than 40 years or more than 74 years were excluded, given the recommendations for target ages of breast cancer screening (13,14). In addition, women who died or developed any type of cancer within 90 days after breast cancer screening were excluded to avoid the possibility of detecting prevalent cancer events through screening.

Exposure and Outcomes of Interest

The mammographic screening results are classified by radiologists (15) into four categories: negative (BI-RADS category 1), benign breast disease (BI-RADS category 2), suspected breast cancer (BI-RADS categories 4 and 5), and incomplete with additional evaluation required (BI-RADS categories 0 and 3) (16), in accordance with guidelines of the Korean National Breast Cancer Screening Program (17,18). As mentioned previously, we included the mammographic results of only women with negative results (BI-RADS category 1), which is considered a normal breast, and women with benign breast disease (BI-RADS category 2).

After breast cancer screening, mammographic breast density was classified using the fourth edition BI-RADS density categories (15). BI-RADS category A is almost entirely fat (parenchyma <25%), category B indicates scattered fibroglandular density (parenchyma is 25%–50%), category C is heterogeneously dense (parenchyma is 51%–75%), and category D is extremely dense (parenchyma >75%) (19).

The primary outcome was a breast cancer event, which was defined as the combination of the International Classification of Diseases 10th Revision, or ICD-10, code of invasive breast cancer (C50), ductal carcinoma in situ (DCIS) (D05), and the catastrophic illness code for cancer (20). The catastrophic illness code is related to the cost sharing of out-of-pocket expenses for diseases with a high financial burden in Korea; thus, catastrophic illness codes for certain diseases have high validity.

Measures of Covariates

The following factors were considered covariates in the present study: age, family history of breast cancer in first-degree relatives, history of benign breast cancer disease, age at menarche, number of children, duration of breastfeeding, breastfeeding history, oral contraceptive use, hormone replacement therapy, smoking history, and number of days of alcohol consumption per week, which were measured through a self-administered questionnaire. In addition, the body mass index (BMI) was calculated using height and weight measured by trained medical staff during the health examination. Self-reported information and BMI were assessed during breast cancer screening.

Statistical Analyses

Descriptive statistics of baseline characteristics of the patients who developed breast cancer and those who were free of breast cancer during follow-up were determined and compared using the χ2 test or Student t test. The probability of developing breast cancer within 5 and 10 years was calculated as the proportion of breast cancer events among participants. The cumulative incidence of breast cancer was calculated using nonparametric methods to account for the competing risk, given the presence of benign breast disease and breast density classifications at baseline. The Gray test was used to compare the cumulative incidence functions (21). Cox proportional hazard regression analysis was conducted to calculate the hazard ratio (HR) and 95% CIs for the combined association of breast density, benign breast disease, and breast cancer risk. HRs were adjusted for other covariates, including age, BMI, age at menarche, menopausal status, age at menopause, parity, breastfeeding, oral contraceptive use, physical activity, alcohol consumption, and smoking status. Stratified subgroup analysis was performed for two subsets of outcomes: invasive breast cancer and DCIS. To assess the combined effect of breast density and benign breast disease on breast cancer risk, we created a dummy variable with eight groups (according to the presence or absence of benign breast disease and four BI-RADS categories of breast density). The reference was women without benign breast disease and breast density category A. In the univariable regression model, only the aforementioned dummy variable was included. Other covariates were added to the multivariable model. All reported P values were two sided with type I error (α < .05) and were considered statistically significant. Statistical analyses were performed using SAS statistical software (version 9.4; SAS Institute).

Results

Characteristics of Study Sample

There were 5 122 000 women who underwent mammographic screening between 2009 and 2010; after exclusions, the final study sample included 3 911 348 women. Among the 3 911 348 women, 58 321 breast cancer events developed during a median follow-up period of 10.6 years (Fig 1). The mean age of the non–breast cancer group was 54.7 years ± 9.6 (SD), and the mean age of the breast cancer group was 51.8 years ± 8.7 (Table 1). Among women who developed breast cancer, a higher proportion of patients exhibited benign breast disease and dense breast at baseline than women who did not develop breast cancer (presence of benign breast disease: 10 729 of 58 321 [18.4%] vs 519 368 of 3 853 027 [13.3%], P < .001; dense breast: 32 296 of 58 321 [55.4%] vs 1 480 867 of 3 853 027 [38.4%], P < .001). Other reproductive- and lifestyle-related characteristics of the study participants are presented in Table 2. Among 3 911 348 women, 263 957 (7%) exhibited both benign breast disease and heterogeneous or extremely dense breasts (BI-RADS density category C or D) (Table E1 [online]). Among women with benign breast disease, the proportion of BI-RADS density categories C and D was higher than that in women without benign breast disease (188 152 of 530 097 [35%] vs 854 051 of 3 381 251 [25%] and 75 805 of 530 097 [14%] vs 395 155 of 3 381 251 [12%], P < .001).

Figure 1: Flow diagram used for selection of the eligible population. BI-RADS = Breast Imaging Reporting and Data System.

Table 1: Baseline Characteristics at Screening Examination of Study Participants

Table 1:

Table 2: Baseline Characteristics Relating of Lifestyle Factors at Screening Examination of Study Participants

Table 2:

Breast Cancer Incidence by Benign Breast Disease Status and Breast Density Categories

Table 3 presents the 5- and 10-year probability of developing breast cancer and the overall incidence rate per person-year according to the presence of benign breast disease and BI-RADS density category. Among women without benign breast disease, the 10-year risk of developing breast cancer was 8332 of 1 136 709 (0.7%) in the BI-RADS density category A group, increasing to 8755 of 395 155 (2.2%) in the BI-RADS density category D group; the corresponding breast cancer incidence rates were 79 and 232 events per 100 000 person-years.

Table 3: Incidence of Breast Cancer by Presence or Absence of Benign Breast Disease

Table 3:

The 10-year risk of developing breast cancer was 1115 of 101 636 (1.1%) in women with benign breast disease and BI-RADS density category A and 2000 of 75 805 (2.6%) in women with benign breast disease and BI-RADS density category D, with corresponding breast cancer incidence rates of 118 and 276 per 100 000 person-years.

Figure 2 presents the cumulative breast cancer incidence curve for the presence of benign breast disease within the breast density group. The cumulative breast cancer incidence was higher in those with benign breast disease, regardless of breast density, during the follow-up period. Differences in the cumulative incidence of breast cancer broadened over time, with a higher risk detected in women with benign breast disease than in women without benign breast disease in all density categories (P < .001). In women without benign breast disease, the probability of developing breast cancer during the 10.6 follow-up years after mammography screening increased corresponding to the breast density level (from 0.94% in women with BI-RADS density category A to 2.68% in women with BI-RADS density category D). A comparable pattern was observed in women with benign breast disease: the risk of developing breast cancer increased from 1.36% in women with BI-RADS density category A to 3.2% in women with BI-RADS density category D.

Cumulative incidence functions of breast cancer risk by breast density                         classification. Dashed lines indicate cumulative incidence function in women                         without benign breast disease, and solid lines indicate cumulative incidence                         function in women with benign breast disease. P values were obtained with                         the Gray test for equality of cumulative incidence functions of the two                         groups. The cumulative breast cancer incidence was higher in those with                         benign breast disease, regardless of breast density. In women with and those                         without benign disease, the probability of developing breast cancer during                         follow-up increased corresponding to the breast density level: (A) 1.4% and                         0.9%, respectively, in BI-RADS A; (B) 1.9% and 1.4%, respectively, in                         BI-RADS B; (C) 2.7% and 2.1%, respectively, in BI-RADS C; and (D) 3.2% and                         2.7%, respectively, in BI-RADS D. BI-RADS = Breast Imaging Reporting and                         Data System.

Figure 2: Cumulative incidence functions of breast cancer risk by breast density classification. Dashed lines indicate cumulative incidence function in women without benign breast disease, and solid lines indicate cumulative incidence function in women with benign breast disease. P values were obtained with the Gray test for equality of cumulative incidence functions of the two groups. The cumulative breast cancer incidence was higher in those with benign breast disease, regardless of breast density. In women with and those without benign disease, the probability of developing breast cancer during follow-up increased corresponding to the breast density level: (A) 1.4% and 0.9%, respectively, in BI-RADS A; (B) 1.9% and 1.4%, respectively, in BI-RADS B; (C) 2.7% and 2.1%, respectively, in BI-RADS C; and (D) 3.2% and 2.7%, respectively, in BI-RADS D. BI-RADS = Breast Imaging Reporting and Data System.

Combined Effects of Benign Breast Disease and Breast Density on Breast Cancer Risk

The presence of benign breast disease was associated with an increased risk of breast cancer across the BI-RADS breast density categories, although the association was lower, corresponding to a higher level of dense breast tissue (Table E2 [online]). The significant P value for heterogeneity indicated that there was an interaction effect between breast density and benign breast disease on the risk of breast cancer (P < .001). Table 4 presents the HRs associated with each combination of baseline benign breast disease status and breast density categories. The presence of both benign breast disease and higher breast density at baseline screening was associated with an elevated risk of breast cancer when compared with that in women with no benign breast disease and BI-RADS density category A. Among women without benign breast disease, the HRs increased as the BI-RADS density category increased, reaching an HR value of 2.28 (95% CI: 2.20, 2.35) in women with BI-RADS density category D. The HR value in women with benign breast disease and BI-RADS density category A was 1.49 (95% CI: 1.40, 1.58) when compared with that in women without benign breast disease and the same density group. In women with benign breast disease and BI-RADS density category D, the HR was 2.75 (95% CI: 2.63, 2.88) when compared with women without benign breast disease and BI-RADS density category A. In addition, multivariable regression results showed significant association with breast cancer risk for the following factors: age at menarche (≥16 years vs <16 years; HR, 0.87; 95% CI: 0.75, 0.89), parity (parous vs nulliparous: HR, 0.78; 95% CI: 0.89, 0.93), breast feeding (ever vs never: HR, 0.91; 95% CI: 0.89, 0.93), family history of breast cancer in first-degree relative (yes vs no: HR, 1.91; 95% CI: 1.82, 2.00), smoking status (ever smoked vs never smoked: HR, 1.03; 95% CI: 1.02, 1.05), and hormone replacement therapy (ever vs never: HR, 0.77; 95% CI: 0.75, 0.79) (data not shown).

Table 4: Breast Cancer Risk by Breast Density and Benign Breast Disease

Table 4:

Subgroup Analysis by Invasive Breast Cancer and DCIS Outcomes

We further assessed the combined effect of benign breast disease and breast density on the risk of invasive breast cancer and DCIS independently (Tables E3, E4, and E5 [online]). Consistent with the primary analysis, the combined effect of benign breast disease and breast density was associated with an increased risk of both invasive breast cancer and DCIS, which increased in parallel with higher breast density.

Discussion

Although mammographic breast density and benign breast disease are considered strong risk factors for developing breast cancer (14), few studies have comprehensively elucidated their combined effects on breast cancer risk. Of 3.9 million mammograms followed over a median of 10.6 years as part of a nationwide breast cancer screening program in Korean women aged at least 40 years, we observed that the combined effect of benign breast disease and Breast Imaging Reporting and Data System (BI-RADS) breast density was positively associated with an elevated breast cancer risk. In this study, 7% of the screened women exhibited both benign breast disease and heterogeneous or extremely dense breasts (BI-RADS density category C or D). The cumulative breast cancer risk increased over time, corresponding with higher levels of breast density in both women with benign breast disease and women with no benign breast disease. The strongest association was observed in women with benign breast disease and extremely dense breasts who presented a 2.75-fold (HR, 2.75; 95% CI: 2.63, 2.88; P < .001) higher risk of developing breast cancer than women without benign breast disease and almost entirely fatty tissue. In addition, women with benign breast disease and scattered fibroglandular densities or heterogeneously dense breasts were associated with a 1.9-fold (HR, 1.93; 95% CI: 1.85, 2.01; P < .001) and 2.4-fold (HR, 2.41; 95% CI: 2.32, 2.50; P < .001) higher risk, respectively, than those without benign breast disease and with entirely fat density.

Our findings confirmed the association between dense breasts and elevated breast cancer risk, which was previously detected in other populations (1,22,23) and in Korean women (24,25). Furthermore, we confirmed the association between benign breast disease and breast cancer risk that has been shown in previous studies. Benign breast disease has been associated with increased breast cancer risk (2,3), with a four-fold increased risk in women with atypia and a two-fold increased risk in women with proliferative lesions (2).

Although both benign breast disease and breast density have been individually proven as well-established and strong risk factors for breast cancer, only a few studies have evaluated the combined effects of these two factors, including a study by Tice et al (26) that used clinical factors and mammographic breast density to estimate breast cancer risk. Also, in the United States, the Breast Cancer Surveillance Consortium reported that the combination of atypical hyperplasia and marked breast density was associated with a five-fold increased risk of developing breast cancer (HR, 5.34; 95% CI: 3.52, 8.09) (6). Another recent study in Spain reported that women with benign breast disease and extremely dense breasts have a three-fold increased risk of breast cancer when compared with those with scattered fibroglandular density and without benign breast disease (HR, 3.07; 95% CI: 2.01, 4.68) (5). However, findings from this study were adjusted only for age at screening, and other covariates were not considered in the analysis, which might have confounded the results by other risk factors of breast cancer. Both aforementioned studies were conducted in settings similar to our study, and the findings were based on data from the screening cohort. In addition, our findings were based on large-scale data using 58 321 detected breast cancer cases and a longer follow-up period than in the previous studies (5,6). Overall, our results are largely consistent with those of previous reports, demonstrating that the combination of benign breast disease and dense breast tissue is associated with an increased risk of future breast cancer.

A history of benign breast disease or past breast biopsy results has been previously implicated as a strong risk factor in most breast cancer risk prediction models, including the modified Gail model from the Breast Cancer Detection Demonstration Project (27,28), Rosner-Colditz model from the Nurses’ Health Study (29,30), the Breast Cancer Surveillance Consortium model (26,31), and the Tyrer-Cuzick model (32,33). However, only the latter two models (ie, the Breast Cancer Surveillance Consortium and Tyrer-Cuzick models) include both benign breast disease and breast density in the risk assessment tool. The increased risk of breast cancer among women with benign breast disease and higher breast density detected in our study provides supportive evidence indicating that these two factors should be incorporated into risk models assessing the future development of breast cancer, as well as in risk-based screening strategies. In our cohort, 7% of screened women exhibited both benign breast disease and heterogeneous or extremely dense breasts (BI-RADS density category C or D). Hence, these women could benefit from more intensive screening strategies and interventions to reduce breast density and subsequently decrease their risk of developing breast cancer.

With consistent findings regarding the increased risk of benign breast disease with dense breasts in this study and previous work (5), women with dense breasts and the presence of benign breast disease would be potential targets for supplemental screening. Findings from a recent clinical trial (34) reported that supplemental MRI screening in women with extremely dense breasts reduced interval cancers compared with mammography alone during a 2-year screening period. A recent clinical trial in Japan also found that supplemental US in addition to mammography increased the sensitivity and early breast cancer detection with fewer interval cancers in young women with dense breasts (35). In addition, Kerlikowske et al (36) suggested that not only breast density but also individuals’ 5-year breast cancer risk should be combined when recommending supplemental screening for women with dense breasts. The National Comprehensive Cancer Network guideline recommends that women aged at least 35 years with an individual 5-year risk of invasive breast cancer of at least 1.7% shorten the screening interval and consider risk-reduction strategies (37). Given the lower breast cancer incidence rate in South Korea compared with that in the United States, women with both benign disease and BI-RADS D did not reach the 1.7% incidence of 5-year risk (1.12% of 5-year invasive breast cancer risk; Table E4 [online]). Meanwhile, the current Korean guidelines for breast cancer state that the available evidence is insufficient to assess the benefits and harms of supplemental US in combination with mammography as a screening modality for breast cancer (35). Although the information on breast density and benign breast disease could be obtained during screening and could then be used to recommend supplemental screening, this approach needs to be considered in South Korea with more evidence from future research.

Our study had limitations. First, our definition of benign breast disease was not based on information from biopsies. Although previous studies on benign breast disease and breast cancer risk defined benign breast disease using information from biopsies (5,6), data from biopsy results were unavailable in the NHIS-NHID in Korea. In the screening setting, if a woman is considered to have benign breast disease at mammography, no further work-up is recommended, and regular mammographic screening according to the recommended interval is not recommended (13). Second, in the Korean National Breast Cancer Screening Program, the interpretation of screening mammograms by at least two radiologists, as provided for in European guidelines (38), is not obligatory. Thus, BI-RADS classification and BI-RADS breast density were interpreted by one radiologist at several screening centers. Although the BI-RADS classification has been widely used, the results may vary depending on the ability and experience of the radiologists. However, in Korea, a mammography education program to standardize the performance of radiologists is available, which might increase the reproducibility of the interpretation (39). Inter-radiologist variability was assessed in randomly selected films from the Korean National Breast Cancer Screening Program, reporting an inter-radiologist variability of 0.83, thus indicating very high agreement (40).

Herein, our results revealed that benign breast disease and breast density increase the risk of developing breast cancer, with a greater than two-fold increased risk in women with benign breast disease and markedly dense breasts. Our findings strengthen the evidence suggesting that benign breast disease and breast density are important factors that should be carefully considered when stratifying breast cancer risk and should be incorporated in future breast cancer risk models. In addition, our findings might help future research in developing a risk-based mammographic screening strategy targeting high-risk groups that might be beneficial in women with benign breast disease and dense breasts. Future research should assess the association stratified by histologic classifications of benign breast disease and determine whether the relationship deviates by molecular subtypes of breast cancer, where the magnitude of association may differ.

Disclosures of conflicts of interest: S.K. No relevant relationships. T.X.M.T. No relevant relationships. H.S. No relevant relationships. S.R. No relevant relationships. Y.C. No relevant relationships. B.P. No relevant relationships.

Author Contributions

Author contributions: Guarantors of integrity of the entire study, S.K., T.X.M.T., S.R., B.P.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of the final version of the submitted manuscript, all authors; agrees to ensure any questions related to the work are appropriately resolved, all authors; literature research, S.K., T.X.M.T., Y.C., B.P.; clinical studies, T.X.M.T., S.R., Y.C., B.P.; statistical analysis, S.K., T.X.M.T., H.S.; and manuscript editing, S.K., T.X.M.T., H.S., Y.C., B.P.

Supported by a National Research Foundation of Korea grant funded by the Korean government (MSIT) (2021R1A2C1011958).

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https://pubs.rsna.org/doi/10.1148/radiol.212727

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