Song 2024 Oi 240423 1715804968.13157

Original Investigation | Oncology
Risk Factors and Mortality Among Women With Interval Breast Cancer
vs Screen-Detected Breast Cancer
Huiyeon Song, MPH; Thi Xuan Mai Tran, PhD; Soyeoun Kim, PhD; Boyoung Park, MD, PhD
Abstract Key Points

Question What are the established risk
IMPORTANCE The risk factors for interval breast cancer (IBC) compared with those for screen-
factors for women with interval breast
detected breast cancer (SBC) and their association with mortality outcomes have not yet been
cancer (IBC) vs screen-detected breast
evaluated among Korean women.
cancer (SBC), and how might they be
associated with mortality outcomes?
OBJECTIVE To evaluate risk factors associated with IBC and survival among Korean women with IBC
compared with those with SBC. Findings In this cohort study of 18 194
Korean women who underwent
DESIGN, SETTING, AND PARTICIPANTS This retrospective cohort study used data from the Korean mammographic breast cancer
National Health Insurance Service Database. Women who participated in a national mammographic screening, breast density, obesity, and
breast cancer screening program between January 1, 2009, and December 31, 2012, were included. hormone replacement therapy use were
Mortality outcomes were calculated from the date of breast cancer diagnosis to the date of death or associated with IBC compared with SBC.
December 31, 2020. Data were analyzed from March 1 to June 30, 2023. Overall mortality of IBC was comparable
with that of SBC.
EXPOSURE Breast cancer diagnosed within 6 to 24 months after a negative screening result (ie, IBC)
Meaning These findings suggest that
or within 6 months after a positive screening result (ie, SBC).
breast density is associated with IBC;
additional research is warranted to
MAIN OUTCOMES AND MEASURES Risk factors and survival rates for IBC and SBC.
determine whether a shortened
screening period and new screening
RESULTS This study included 8702 women with IBC (mean [SD] age, 53.3 [8.6] years) and 9492
strategies are needed for women with
women with SBC (mean [SD] age, 54.1 [9.0] years). Compared with SBC, the probability of IBC
risk factors for IBC.
decreased as mammographic density increased. Lower body mass index, menopausal status,
hormone replacement therapy (HRT) use, and lack of family history of breast cancer were associated
with a higher likelihood of IBC. When stratified by detection time, younger age at breast cancer + Supplemental content
diagnosis and family history of breast cancer were associated with an increased likelihood of IBC Author affiliations and article information are
diagnosed at 6 to 12 months but a decreased likelihood of IBC diagnosed at 12 to 24 months. Overall listed at the end of this article.
mortality of IBC was comparable with SBC, but total mortality and cancer-related mortality of IBC
diagnosed between 6 and 12 months was higher than that of SBC.
CONCLUSIONS AND RELEVANCE The findings of this cohort study suggest that breast density,
obesity, and HRT use were associated with IBC compared with SBC. These findings also suggest that
higher supplemental breast ultrasound use among Korean women, especially those with dense
breasts, could be attributed to a lower incidence of IBC among women with dense breasts compared
with women with SBC, due to greater detection. Finally, overall mortality of IBC was comparable with
that of SBC.
JAMA Network Open. 2024;7(5):e2411927. doi:10.1001/jamanetworkopen.2024.11927
Open Access. This is an open access article distributed under the terms of the CC-BY License.
JAMA Network Open. 2024;7(5):e2411927. doi:10.1001/jamanetworkopen.2024.11927 (Reprinted) May 20, 2024 1/13
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JAMA Network Open | Oncology Risk Factors and Mortality Among Women With Interval vs Screen-Detected Breast Cancer
Introduction
According to GLOBOCAN estimates, female breast cancer was the most common incident cancer
type in 2020, with approximately 2.3 million new cases, accounting for 24.5% of all cancer
diagnoses.1 In Korea, breast cancer is the most common cancer type in women aged 35 to 64 years,
and its incidence has been increasing since nationwide cancer statistics were first reported in 1999.2
To reduce the burden of breast cancer through early detection and treatment, mammographic breast
cancer screening is recommended for average-risk women in many countries.3 In Korea,
mammography is provided biennially to women aged 40 years or older as a nationwide organized
screening program.4
Breast cancer diagnosed after a negative screening but before the next scheduled mammogram
is referred to as interval breast cancer (IBC).5,6 There are 2 types: (1) “true” IBC, in which cancer did
not present on the previous mammogram and thus developed during the screening interval; and (2)
tumors missed on the previous mammogram (ie, false-negative results).5 Compared with screen-
detected breast cancer (SBC), IBC has more aggressive characteristics and a worse prognosis.5
Previous studies have identified the following risk factors for IBC: high breast density, current
hormone replacement therapy (HRT) use, young age, premenopausal status, and family history of
breast cancer.7 Previous studies focused on IBC risk factors and characteristics have been conducted
mainly in Western countries, where early mammographic breast cancer screening is recommended.
However, little is known about the risk factors for IBC among Asian women.
Identification of epidemiologically associated risk factors for IBC and survival rates of Asian
women with IBC compared with those with SBC would be useful for improving screening strategies
for women in Asia. Therefore, this study aimed to compare established risk factors for IBC and SBC
among Korean women using data from a nationwide mammographic screening program.
Furthermore, mortality outcomes of IBC were compared with those of SBC.
Methods
The institutional review board of Hanyang University College of Medicine, Republic of Korea,
approved the protocol for this cohort study. In addition, the National Health Insurance Sharing
Service System (NHIS) approved the use of the NHIS database, which was constructed after
individual identities were anonymized. The need for informed consent was thus waived due to
secondary data analysis. The study followed the Strengthening the Reporting of Observational
Studies in Epidemiology (STROBE) reporting guideline.
Study Design and Population

This study used data from the National Health Insurance Service National Health Information
Database (NHIS-NHID). As a single compulsory health insurance system in Korea, the NHIS-NHID
includes information on demographics, health care use, vital statistics, and national health screening
results for the entire Korean population.8
This study included data from all women who underwent national mammographic breast
cancer screening between January 1, 2009, and December 31, 2012 (Figure). The mammographic
screening film was read by a trained radiologist and the results were recorded according to the Breast
Imaging Reporting and Data System, Fourth Edition (BI-RADS 4). A positive screening result was
defined as a BI-RADS final assessment of 0, 4, or 5 (incomplete, suspicious abnormality, or highly
suggestive of malignancy), and negative screening results were defined as 1, 2, or 3 (negative, benign
finding, or probably benign) based on the American College of Radiology guideline.9 Participants
were excluded if they met the following criteria: (1) were younger than 40 years or aged 75 years or
older at the time of screening (n = 347 845), according to the recommended age in Korean guidelines
for breast cancer screening10; (2) had a history of breast cancer before the mammographic screening
date (n = 27); (3) were missing information on breast cancer screening results (n = 45); (4) were

missing information on mammographic breast density (n = 147 259); or (5) had received any type of
cancer diagnosis before screening (n = 179 128). Of the 6 772 811 women screened, 5 628 035 had
negative results and 1 144 776 had positive results.
Definition of IBC and SBC

Breast cancer was defined as any breast cancer event according to International Classification of
Diseases, Tenth Edition (ICD-10) codes for invasive breast cancer (C50.0-C50.9) and ductal carcinoma
in situ (D05.0-D05.9) and as any cancer event registered with the rare incurable disease code for
cancer. If a breast cancer diagnosis occurred within 6 months from the date of mammographic
screening among women with positive screening results, the case was defined as SBC, considering
the time of referral to a hospital for further examination and pathologic confirmation. The 6-month
period to define SBC was applied in another claim-based study in Korea.11 Among women with
negative screening results, cancers diagnosed within the first 6 months after negative screening
were considered false-negative results and were excluded. Considering the definition of IBC and the
screening cycle of other studies,12-14 the case was defined as IBC if the diagnosis of breast cancer
occurred during the period 6 to 24 months after negative breast cancer screening. Considering the
recommendation of annual breast cancer screening in other guidelines,3 IBC was further classified as
breast cancer diagnosed either 6 to 12 months or 12 to 24 months after negative screening. Breast
cancer was defined as a combination of the ICD-10 codes for invasive breast cancer and ductal
carcinoma in situ and the special code for cancer.15 Based on this definition, we identified 8702
women with IBC (2359 were diagnosed between 6 and 12 months after negative screening, and 6343
were diagnosed between 12 and 24 months) from 5 628 035 with negative results (0.15%) and 9492
women with SBC from 1 144 776 with positive results (0.83%).
Established Risk Factors for Breast Cancer Considered in This Study

During cancer screening, participants were asked to complete a self-administered questionnaire
about their health behaviors and risk factors for breast cancer. The following risk factors were
considered in this study: age at diagnosis (40-49, 50-59, or 60-74 years), mammographic density
according to BI-RADS 4 category (1, <25% glandular; 2, 25%-50% glandular; 3, 51%-75% glandular;
Figure. Study Flow Diagram
7 447 115 Women received mammographic breast

cancer screening (January 1, 2009, through
December 31, 2012)
674 304 Excluded

347 845 Aged <40 or >74 y at screening
179 128 Died or diagnosed with any type of cancer before screening
147 259 Missing information on mammographic breast density
45 Missing information on breast cancer screening results
27 History of breast cancer before screening
6 772 811 Participants included in the analysis
5 628 035 With negative breast cancer 1 144 776 With positive breast cancer
screening results screening results
8702 With interval breast cancer diagnosed 9492 With screening-detected breast
within 6-24 mo after screening cancer diagnosed within 6 mo
2359 With interval breast cancer 6343 With interval breast cancer
detected between 6 and 12 mo detected between 12 and 24 mo

or 4, >75% glandular), body mass index (BMI [calculated as weight in kilograms divided by height in
meters squared]; underweight, <18.5; normal, 18.5 to <23.0; overweight, 23.0 to <25.0; or obesity,
ⱖ25.0), age at menarche (<15, 15-16, or ⱖ17 years), menopausal status (premenopausal or
postmenopausal), oral contraceptive use (never or ever), HRT use after menopause (never or ever),
parity (nulliparous, primiparous, or multiparous), breastfeeding experience (never or ever), family
history of breast cancer in first-degree relatives (no or yes), current alcohol consumption (no or yes
[<1 or ⱖ1 per week during the last year]), and physical activity (no or yes [<1 or ⱖ1 time per week at
time of screening]).
Mortality
Mortality and causes of death of individuals between 2009 and 2020 were confirmed by linking the
NHIS-NHID data with mortality data from the Korea National Statistical Office (KNSO) using a unique
13-digit resident registration number. The KNSO death certificate includes the cause of death
according to the ICD-10 code and the date of death. First, all-cause mortality, defined as death from
any cause, was assessed. Causes of death were classified as breast cancer–related death (recorded
cause of death as breast cancer) or deaths other than breast cancer (all other causes). Moreover,
causes of death were also classified into cancer-related deaths (recorded causes of death as any
cancer) and deaths other than cancer (all other causes).
Statistical Analysis
Descriptive statistics on breast cancer risk factors among women with SBC or IBC were compared
using the t test or χ2 test. Continuous variables are presented as means with SDs, and categorical
variables are presented as numbers with percentages. Logistic regression with the aforementioned
established risk factors for breast cancer was used to identify epidemiologically associated factors for
IBC compared with SBC. Odds ratios (ORs) and 95% CIs for each factor with and without adjustments
for other factors are presented. Analysis was performed for all participants with IBC and stratified by
IBC diagnosed between 6 and 12 months and between 12 and 24 months. Given that mammographic
density could affect IBC itself and its association with other factors,16 a multiple logistic regression
analysis of the association between established risk factors for breast cancer and IBC compared with
SBC was performed, stratified by breast density (nondense [BI-RADS density categories 1-2] and
dense [BI-RADS density categories 3-4]).
Mortality outcomes for IBC compared with SBC were analyzed using Cox proportional hazards
regression analysis. Follow-up for the mortality outcome was calculated from the date of breast
cancer diagnosis to the date of death or December 31, 2020. Hazard ratios (HRs) for mortality risk are
presented as unadjusted, adjusted for age at diagnosis, and adjusted for all of the aforementioned
known risk factors for breast cancer for all-cause mortality, breast cancer–related death, cancer-
related death, deaths other than breast cancer, and deaths other than cancer. A 2-sided P < .05 was
considered statistically significant. Statistical analysis was performed with SAS, version 9.4 (SAS
Institute). Data were analyzed from March 1 to June 30, 2023.
Results
Characteristics of Women With IBC vs SBC
A total of 18 194 women were included in the study; 9492 had SBC and 8702 had IBC (Table 1). Of the
8702 women with IBC, 2359 (27.1%) were diagnosed between 6 and 12 months after negative breast
cancer screening and 6343 (72.9%) were diagnosed between 12 and 24 months. Women with IBC
were younger at the time of cancer diagnosis (mean [SD] age, 53.3 [8.6] years) compared with those
with SBC (mean [SD] age, 54.1 [9.0] years). The proportion of BI-RADS category 4 tumors was higher
for women with IBC (2031 [23.3%]) compared with those with SBC (1895 [20.0%]). Compared with
women with SBC, a lower proportion of women with IBC had obesity (2590 [29.8%] vs 3328 [35.1%])
and a higher proportion of women with IBC used HRT (768 [18.2%] vs 750 [14.3%]). Proportions of

Table 1. Characteristics of the IBC and SBC Groupsa
Cancer type IBC diagnostic periodb

c
Risk factor SBC (n = 9492) IBC (n = 8702) P value 6-12 mo (n = 2359) 12-24 mo (n = 6343) P valuec
Age at diagnosis, y
Mean (SD) 54.1 (9.0) 53.3 (8.6) <.001 52.2 (8.4) 53.7 (8.7) .13
40-49 3282 (34.6) 3342 (38.4) 1058 (44.9) 2284 (36.0)
50-59 3558 (37.5) 3303 (38.0) <.001 856 (36.3) 2447 (38.6) <.001
60-74 2652 (27.9) 2057 (23.6) 445 (18.9) 1612 (25.4)
BI-RADS breast density categoryd
1 1222 (12.9) 1231 (14.2) 299 (12.7) 932 (14.7)
2 2554 (26.9) 2120 (24.4) 521 (22.1) 1599 (25.2)
<.001 <.001
3 3821 (40.3) 3320 (38.2) 943 (40.0) 2377 (37.5)
4 1895 (20.0) 2031 (23.3) 596 (25.3) 1435 (22.6)
BMI
Underweight (<18.5) 187 (2.0) 213 (2.5) 68 (2.9) 145 (2.3)
Normal (18.5-23) 3648 (38.4) 3702 (42.5) 1032 (43.8) 2670 (42.1)
Overweight (23-25) 2328 (24.5) 2196 (25.2) <.001 597 (25.3) 1599 (25.2) .08
Obesity (≥25) 3328 (35.1) 2590 (29.8) 662 (28.1) 1928 (30.4)
Missing 1 (0) 1 (0) 0 1 (0)
Age at menarche, y
<15 2798 (29.5) 2774 (31.9) 773 (32.8) 2001 (31.6)
15-16 4018 (42.3) 3690 (42.4) 989 (41.9) 2701 (42.6)
<.001 .65
≥17 2435 (25.7) 2039 (23.4) 548 (23.2) 1491 (23.5)
Missing 241 (2.5) 199 (2.3) 49 (2.1) 150 (2.4)
Menopausal status
Premenopause 4123 (43.4) 4390 (50.5) 1250 (53.0) 3140 (49.5)
Postmenopause 5256 (55.4) 4212 (48.4) <.001 1086 (46.0) 3126 (49.3) .01
Missing 113 (1.2) 100 (1.2) 23 (1.0) 77 (1.2)
Oral contraceptive use
Never 7502 (79.0) 6983 (80.3) 1901 (80.6) 5082 (80.1)
Ever 1373 (14.5) 1195 (13.7) .12 321 (13.6) 874 (13.8) .85
Missing 617 (6.5) 524 (6.0) 137 (5.8) 387 (6.1)
HRT use among postmenopausal women
Never 3570 (67.9) 2637 (62.6) 684 (63.0) 1953 (62.5)
Ever 750 (14.3) 768 (18.2) <.001 197 (18.1) 571 (18.3) .95
Missing 936 (17.8) 807 (19.2) 205 (18.9) 602 (19.3)
Parity
Nulliparous 634 (6.7) 542 (6.2) 159 (6.7) 383 (6.0)
Primiparous 1389 (14.6) 1228 (14.1) 354 (15.0) 874 (13.8)
.41 .005
Multiparous 7354 (77.5) 6828 (78.5) 1821 (77.2) 5007 (78.9)
Missing 115 (1.2) 104 (1.2) 25 (1.1) 79 (1.3)
Breastfeeding experience
Never 1598 (16.8) 1669 (19.2) 484 (20.5) 1185 (18.7)
Ever 7611 (80.2) 6792 (78.1) <.001 1815 (76.9) 4977 (78.5) .13
Missing 283 (3.0) 241 (2.8) 60 (2.5) 181 (2.9)
Family history of breast cancer
No 8790 (92.6) 8136 (93.5) 2157 (91.4) 5979 (94.3)
.02 <.001
Yes 702 (7.4) 566 (6.5) 202 (8.6) 364 (5.7)
Current alcohol consumption
No 7473 (78.7) 6639 (76.3) 1779 (75.4) 4860 (76.6)
Yes 1972 (20.8) 2021 (23.2) <.001 571 (24.2) 1450 (22.9) .31
Missing 47 (0.5) 42 (0.5) 9 (0.4) 33 (0.5)
(continued)

Table 1. Characteristics of the IBC and SBC Groupsa (continued)
Cancer type IBC diagnostic periodb

c
Risk factor SBC (n = 9492) IBC (n = 8702) P value 6-12 mo (n = 2359) 12-24 mo (n = 6343) P valuec
Physical activity
No 2563 (27.0) 2275 (26.1) 579 (24.5) 1696 (26.7)
Yes 6868 (72.4) 6380 (73.3) .27 1767 (74.9) 4613 (72.7) .12
Missing 61 (0.6) 47 (0.5) 13 (0.6) 34 (0.5)
Abbreviations: BI-RADS, Breast Imaging Reporting and Data System; BMI, body mass index (calculated as weight in kilograms divided by height in meters squared); HRT, hormone
replacement therapy; IBC, interval breast cancer; SBC, screen-detected breast cancer.
a
Unless indicated otherwise, values are presented as No. (%) of patients.
b
Subdivided by diagnosis time: within 6 and 12 months and 12 and 24 months.
c
χ2 test for categorical variables and t test for continuous variables.
d
Breast density category 1 was almost entirely fat (<25% glandular), category 2 indicated scattered fibroglandular density (25%-50% glandular), category 3 was heterogeneously
dense (51%-75% glandular), and category 4 was extremely dense (>75% glandular).
younger women, women with dense breasts, premenopausal women, and women with a family
history of breast cancer were lower among women with IBC diagnosed at 12 to 24 months compared
with at 6 to 12 months.
Risk Factors for IBC vs SBC

Table 2 presents established risk factors for breast cancer that were differentially associated with IBC
relative to SBC. We observed that compared with SBC, as the BI-RADS mammographic density
category increased, the probability of IBC decreased in women with density category 2 (adjusted OR
[AOR], 0.76 [95% CI, 0.69-0.84]), category 3 (AOR, 0.70 [95% CI, 0.64-0.78]), and category 4
(AOR, 0.80 [95% CI, 0.72-0.90]) vs density category 1. Compared with women with obesity, lower
BMI was associated with a higher likelihood of IBC among women with overweight (AOR, 1.19 [95%
CI, 1.10-1.29]), normal weight (AOR, 1.24 [95% CI, 1.16-1.34]), and underweight (AOR, 1.36 [95% CI,
1.10-1.67]). For menopause and ever use of HRT after menopause, AORs of 1.21 (95% CI, 1.07-1.35) and
1.40 (95% CI, 1.25-1.57) were observed for IBC vs SBC. For family history of breast cancer and alcohol
consumption, AORs of 0.89 (95% CI, 0.79-0.99) and 1.10 (95% CI, 1.02-1.18) were observed for IBC
vs SBC.
Decreased BI-RADS breast density category, lower BMI, and HRT use after menopause had an
increased association with IBC compared with SBC, regardless of the diagnostic period after negative
screening (6-12 and 12-24 months). However, age group and family history of breast cancer had
different directions of association with IBC diagnostic period after negative screening. Younger age
and family history of breast cancer were associated with an increased likelihood of IBC diagnosis at 6
to 12 months but with a decreased likelihood of IBC diagnosis at 12 to 24 months. When stratified by
breast density (dense and nondense), associations of breast cancer risk factors with IBC, IBC
diagnosed within 6 to 12 months, and IBC diagnosed within 12 to 24 months (eTables 1-3 in
Supplement 1) were comparable with overall risk (Table 2).
Mortality Risk Among Women With IBC vs SBC

The mean (SD) follow-up period after breast cancer diagnosis was 8.4 (1.9) years for women with IBC
and 9.5 (2.1) years for those with SBC. Table 3 presents mortality outcomes among women with IBC
compared with those with SBC. After adjusting for other covariates, no statistically significant
increase or decrease in risk of death from all causes, breast cancer–related death, deaths other than
breast cancer, or deaths other than cancer was observed for IBC compared with SBC. However, IBC
had a 1.12-fold (95% CI, 1.01-1.24) higher risk of cancer-related death. When IBC was stratified by
diagnostic period after a negative screening result, IBC diagnosed within 6 to 12 months had a 1.18-
fold (95% CI, 1.02-1.37) higher risk of death from all causes, a 1.19-fold (95% CI, 1.01-1.41) higher risk of
breast cancer–related death, and a 1.20-fold (95% CI, 1.03-1.40) increased risk of cancer-related

Table 2. Risk Factors for IBC vs SBC
IBC vs SBC (n = 8702) IBC at 6-12 mo vs SBC (n = 2359)a IBC at 12-24 mo vs SBC (n = 6343)a
Risk factor COR (95% CI) AOR (95% CI)b COR (95% CI) AOR (95% CI)b COR (95% CI) AOR (95% CI)b
Age at diagnosis, y
40-49 1.31 (1.22-1.42) 1.00 (0.89-1.12) 1.92 (1.70-2.17) 1.76 (1.48-2.10) 1.15 (1.06-1.24) 0.81 (0.72-0.92)
50-59 1.20 (1.11-1.29) 1.11 (1.02-1.20) 1.43 (1.27-1.63) 1.42 (1.24-1.63) 1.13 (1.04-1.23) 1.02 (0.93-1.11)
60-74 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference]
BI-RADS breast densityc
1 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference]
2 0.82 (0.75-0.91) 0.76 (0.69-0.84) 0.83 (0.71-0.98) 0.74 (0.63-0.87) 0.82 (0.74-0.91) 0.76 (0.69-0.85)
3 0.86 (0.79-0.95) 0.70 (0.64-0.78) 1.01 (0.87-1.17) 0.75 (0.64-0.87) 0.82 (0.74-0.90) 0.68 (0.61-0.76)
4 1.06 (0.96-1.18) 0.80 (0.72-0.90) 1.29 (1.10-1.50) 0.84 (0.71-1.01) 0.99 (0.89-1.11) 0.78 (0.69-0.89)
BMI
Underweight (<18.5) 1.46 (1.20-1.79) 1.36 (1.10-1.67) 1.83 (1.37-2.44) 1.53 (1.14-2.06) 1.34 (1.07-1.68) 1.29 (1.02-1.62)
Normal (18.5-23) 1.30 (1.22-1.40) 1.24 (1.16-1.34) 1.42 (1.28-1.59) 1.25 (1.12-1.40) 1.26 (1.17-1.36) 1.24 (1.14-1.34)
Overweight (23-25) 1.21 (1.12-1.31) 1.19 (1.10-1.29) 1.29 (1.14-1.46) 1.23 (1.08-1.34) 1.19 (1.09-1.29) 1.18 (1.08-1.29)
Obesity (≥25) 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference]
Age at menarche, y
<15 1.18 (1.09-1.28) 1.07 (0.98-1.16) 1.23 (1.09-1.39) 0.97 (0.85-1.10) 1.17 (1.07-1.27) 1.11 (1.01-1.22)
15-16 1.10 (1.02-1.18) 1.02 (0.95-1.10) 1.09 (0.97-1.23) 0.95 (0.84-1.07) 1.10 (1.01-1.19) 1.05 (0.97-1.14)
≥17 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference]
Menopausal status
Premenopause 1.33 (1.25-1.41) 1.21 (1.07-1.35) 1.47 (1.34-1.61) 1.06 (0.88-1.27) 1.28 (1.20-1.37) 1.27 (1.12-1.44)
Postmenopause 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference]
Oral contraceptive use
Never 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference]
Ever 0.94 (0.86-1.02) 0.93 (0.86-1.02) 0.92 (0.81-1.05) 0.94 (0.82-1.08) 0.94 (0.86-1.03) 0.93 (0.85-1.02)
HRT use among
postmenopausal women
Never 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference]
Ever 1.39 (1.24-1.55) 1.40 (1.25-1.57) 1.37 (1.15-1.64) 1.39 (1.16-1.66) 1.39 (1.23-1.57) 1.40 (1.24-1.58)
Parity
Nulliparous 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference]
Primiparous 1.03 (0.91-1.19) 1.00 (0.86-1.17) 1.02 (0.82-1.25) 0.95 (0.76-1.20) 1.04 (0.89-1.21) 1.03 (0.87-1.21)
Multiparous 1.09 (0.96-1.22) 1.12 (0.97-1.28) 0.99 (0.82-1.18) 1.02 (0.83-1.25) 1.13 (0.99-1.29) 1.16 (0.99-1.35)
Breastfeeding experience
Never 1.17 (1.09-1.26) 1.07 (0.99-1.16) 1.27 (1.13-1.42) 1.09 (0.97-1.23) 1.13 (1.04-1.23) 1.06 (0.97-1.16)
Ever 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference]
Family history of breast cancer
No 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference] 1 [Reference]
Yes 0.87 (0.78-0.98) 0.89 (0.79-0.99) 1.17 (1.00-1.38) 1.18 (1.00-1.39) 0.76 (0.67-0.87) 0.77 (0.68-0.88)
Current alcohol consumption
Yes 1.15 (1.08-1.24) 1.10 (1.02-1.18) 1.22 (1.09-1.35) 1.09 (0.98-1.22) 1.13 (1.05-1.22) 1.11 (1.02-1.20)
Physical activity
Yes 1.05 (0.98-1.12) 1.02 (0.95-1.09) 1.14 (1.03-1.26) 1.10 (0.99-1.22) 1.02 (0.95-1.09) 0.99 (0.92-1.06)
Abbreviations: AOR, multivariate-adjusted odds ratio; BI-RADS, Breast Imaging Reporting and Data System; BMI, body mass index (calculated as weight in kilograms divided by height
in meters squared); COR, crude odds ratio; HRT, hormone replacement therapy; IBC, interval breast cancer; SBC, screen-detected breast cancer.
a
Subdivided by diagnosis time: within 6 and 12 months and 12 and 24 months.
b
Multivariate logistic regression model adjusted for age at diagnosis, BI-RADS breast density, BMI, age at menarche, menopausal status, oral contraceptive use, HRT use among
postmenopausal women, parity, breastfeeding experience, family history of breast cancer in first-degree relatives, alcohol consumption, and physical activity.
c
Breast density category 1 was almost entirely fat (<25% glandular), category 2 indicated scattered fibroglandular density (25%-50% glandular), category 3 was heterogeneously
dense (51%-75% glandular), and category 4 was extremely dense (>75% glandular).

deaths compared with SBC. Otherwise, increased mortality or cause-specific mortality was not
observed for IBC at 12 to 24 months compared with SBC.
Discussion
This study investigated differences in risk factors associated with IBC compared with those
associated with SBC and mortality outcomes between IBC and SBC among Korean women who
participated in a nationwide breast cancer screening program. In this study, increased breast density
was associated with a lower likelihood of IBC; however, decreased BMI, HRT use after menopause,
and alcohol consumption were associated with an increased likelihood of IBC compared with SBC.
Age and family history of breast cancer had different associations according to the IBC diagnostic
period after negative screening results. Younger age at the time of breast cancer diagnosis and family
history of breast cancer were associated with an increased likelihood of IBC diagnosis 6 to 12 months
after negative screening results but with a decreased likelihood of IBC diagnosis at 12 to 24 months.
The association between HRT use after menopause and increased risk of IBC has been well
identified in previous studies.7,16-18 Studies have reported that rates of IBC increase with an increasing
duration of HRT use, and the association between HRT use and IBC is greater than that between HRT
and SBC.19,20 In previous studies, lower BMI was associated with a higher risk of IBC diagnosed within
12 months.20-22 Previous studies have reported a higher proportion of premenopausal women with
IBC than women with SBC.23,24 These associations are consistent with the results of this study. The
mechanisms of the previous studies underlying the associations among HRT use, lower BMI,
premenopause, and IBC were mainly explained by the effect of these factors on dense breasts and
the masking effect or independent increased risk of IBC due to higher breast density.22,25 However,
Table 3. Mortality Among Women With IBC vs SBC
HR (95% CI)
Outcome SBC IBCa IBC at 6-12 mo IBC at 12-24 mo
Death from all causes
No. NA 1356 941 1173
Model 1b 1 [Reference] 1.03 (0.94-1.14) 1.09 (0.94-1.26) 1.01 (0.91-1.13)
Model 2c 1 [Reference] 1.06 (0.96-1.16) 1.15 (0.99-1.33) 1.03 (0.92-1.14)
Model 3d 1 [Reference] 1.09 (0.99-1.20) 1.18 (1.02-1.37) 1.05 (0.94-1.17)
Breast cancer–related deaths
No. NA 929 648 793
Model 1 1 [Reference] 1.01 (0.90-1.13) 1.13 (0.96-1.34) 0.96 (0.85-1.09)
Model 2 1 [Reference] 1.02 (0.91-1.14) 1.15 (0.97-1.36) 0.97 (0.85-1.10)
Model 3 1 [Reference] 1.06 (0.94-1.19) 1.19 (1.01-1.41) 1.01 (0.89-1.15)
Deaths other than breast cancer
No. NA 427 293 380 Abbreviations: HR, hazard ratio; IBC, interval breast
Model 1 1 [Reference] 1.09 (0.90-1.32) 0.96 (0.71-1.30) 1.15 (0.93-1.41) cancer; NA, not applicable; SBC, screen-detected
Model 2 1 [Reference] 1.17 (0.97-1.42) 1.31 (0.83-1.53) 1.19 (0.97-1.46) breast cancer.
a
Model 3 1 [Reference] 1.18 (0.98-1.43) 1.13 (0.83-1.53) 1.20 (0.97-1.48) Subdivided into 2 groups according to diagnosis
time: within 6 and 12 months and 12 and 24 months.
Cancer-related deaths
b
Model 1: IBC as the outcome without adjustment.
No. NA 1105 758 949
c
Model 2: IBC as the outcome, adjusted for age at
Model 1 1 [Reference] 1.06 (0.96-1.18) 1.13 (0.96-1.32) 1.03 (0.93-1.17)
diagnosis.
Model 2 1 [Reference] 1.08 (0.97-1.20) 1.17 (1.00-1.36) 1.05 (0.93-1.17)
d
Model 3: IBC as the outcome, adjusted for age at
Model 3 1 [Reference] 1.12 (1.01-1.24) 1.20 (1.03-1.40) 1.09 (0.97-1.22)
diagnosis; Breast Imaging Reporting and Data
Deaths other than cancer System, Fourth Edition breast density; body mass
No. NA 251 183 224 index; age at menarche; menopausal status; oral
Model 1 1 [Reference] 0.84 (0.63-1.10) 0.87 (0.56-1.33) 0.82 (0.60-1.13) contraceptive use; hormone replacement therapy
Model 2 1 [Reference] 0.91 (0.69-1.20) 1.05 (0.68-1.61) 0.86 (0.63-1.17) experience; parity; breastfeeding experience; family
history of breast cancer in first-degree relatives;
Model 3 1 [Reference] 0.91 (0.69-1.21) 1.06 (0.69-1.63) 0.86 (0.63-1.18)
alcohol consumption; and physical activity.

associations between these factors and IBC compared with SBC after adjusting for breast density or
stratified by breast density suggested independent associations with IBC.
A notable finding of this study was the inverse association between increased breast density
and the risk of IBC. Previous studies have consistently reported that increased mammographic
density in terms of BI-RADS categories, density percentage, or dense area was associated with an
increased risk of IBC compared with SBC,5,21,26 which is contrary to the results of this study.16
Increased IBC risk among women with dense breasts or subtle false-negative findings on
mammography may be attributed to the masking effect just described. One study suggested that
only 42.5% of IBC cases were true IBC, 16.2% were false-negative results, and the remaining 41.2%
included occult tumors or minimal signs or were unclassifiable.17 Another Korean study suggested
that 32.5% of IBC cases could be classified as true IBC, 35% as false-negative results (missed
cancers), and 32.5% as minimal signs.26 To reduce the possibility that missed cancer cases were
included in IBC in this study, IBC was stratified by diagnostic period; however, the inverse association
remained, contrary to previous studies.
Despite limited evidence of the benefits of supplemental breast ultrasound screening, breast
ultrasonography in addition to mammography has made a substantial contribution to finding more
breast cancer cases that would be missed by mammography alone in women with dense breasts.27
Another study showed similar IBC rates in women with dense breasts who underwent supplemental
ultrasound screening as in women with nondense breasts.28 A clinical trial in Japan reported that the
IBC rate was lower in women who underwent additional ultrasonography than in those who did not,
regardless of breast density.29 Furthermore, in groups receiving supplemental ultrasonography, IBC
rates were similar in women with dense and nondense breasts.29 Therefore, if women with dense
breasts receive supplemental screening, IBC could be lower than in women with nondense breasts
without supplemental examination. A nationwide survey in Korea reported that breast
ultrasonography was performed extensively in women. A total of 42.1% of women aged 30 years or
older received breast ultrasound and of those who received breast cancer screening, more than 50%
had received breast ultrasound.30 In this study, we were unable to identify whether women in the
high-density category received additional supplemental screening; however, considering that breast
ultrasound is widely performed in Korea, it could be expected that a higher proportion of women
with dense breasts would undergo additional breast ultrasound examinations, which presents an
inverse association between the increase in density category and decrease in IBC. Thus, the
contrasting results from previous studies might be attributed to health service use among Korean
women and not to biological mechanisms.
An increased risk of IBC is associated with younger age compared with older age.7 Similarly, in
our analysis stratified by diagnostic period (6-12 and 12-24 months), the crude OR suggested an
increased risk of IBC in younger women than in older women. However, the multivariate analysis
suggested that an increased risk of IBC was associated with younger age for IBC diagnosed at 6 to 12
months, whereas the opposite association was observed for IBC diagnosed at 12 to 24 months.
Additionally, an opposite association was observed between the unadjusted OR and AOR in IBC
diagnosed at 12 to 24 months compared with SBC, which was attributed to the confounding effect
of menopausal status. Otherwise, premenopausal status, which had a significantly higher risk in the
univariate analysis in both periods, showed only an increased association with IBC diagnosed at
12 to 24 months in the multivariate analysis. Owing to the close association between age and
menopause, adjusting for one factor could affect the association of other factors with the risk of IBC.
In this study, a family history of breast cancer, which is known to be associated with an increased
risk of IBC,7 had an increased association with IBC diagnosed at 6 to 12 months but a decreased
association with IBC diagnosed at 12 to 24 months. In clinical guidelines, a more intensive screening
is recommended at short intervals.31,32 These guidelines affect screening uptake behaviors, leading
to increased IBC at 6 to 12 months and decreased IBC at 12 to 24 months.
In this study, we did not observe differences in overall mortality and cause-specific mortality
between the SBC and IBC groups. However, IBC diagnosed 6 to 12 months after negative screening

showed higher all-cause, breast cancer–related, and cancer-related mortality than SBC, suggesting
the more aggressive nature of IBC diagnosed earlier after negative screening. Studies on the
mortality of IBCs compared with SBCs have shown inconsistent results. For instance, IBCs are
associated with a significantly higher unadjusted risk of breast cancer–related death than SBCs.33 In
addition, IBCs have a significantly worse survival rate than SBCs in women with nondense breasts.5
The reasons for lower survival rates of IBC (<1 year) compared with SBC have been suggested to be
greater tumor size, more aggressive nature (eg, more lymph node involvement), and a higher
proportion of lobular histologic characteristics.5,13,34,35 However, recent studies have not reported
differences in long-term survival between SBCs and IBCs.36 One study reported that except for the
slightly larger size of IBC, the tumor characteristics of SBC and IBC were comparable.37 Because our
population-based screening study could not compare the tumor characteristics of IBC and SBC,
further hospital-based studies with available tumor information should be conducted.
Strengths and Limitations

One strength of our study is that it was a large population-based study of women undergoing breast
cancer screening. However, this study has some limitations. First, despite several previous studies
defining IBC as cancer present after negative screening results and before the next scheduled
screening,7 considering 20% of 25% of IBC cases are classified as false-negative results, we excluded
breast cancers detected after less than 6 months of a negative result to exclude the possibility of
missed cancer (false negative). However, considering that 10% to 30% of mammograms could have
false-negative results due to technical or interpretive errors,37-41 some missed breast cancers could
be included. Due to the unavailability of mammography films, we were unable to evaluate missed
cancer or true IBC. In addition, we did not consider censoring the follow-up for breast cancer at the
next screening, although screening intervals may be shorter for women with a family history of breast
cancer. Therefore, screen-detected IBCs were not eliminated within the 24-month follow-up period
of the previous screening test. Second, the sensitivity and specificity of mammographic screening
varied depending on the reader and type of equipment, such as film or digital mammography.
Despite inter- and intraradiologist variations, the bias was nondifferential, resulting in a net
association with the null hypothesis.42 Therefore, the results observed in this study are robust. In
addition, the inverse association observed between breast density and IBC might be an artifact of the
ultrasound examination; however, we could not control for the use of additional ultrasound
examinations because of unavailable information. Finally, when comparing mortality, information on
tumor characteristics, stage, and treatment methods for IBC and SBC was not considered.
Conclusions
In this cohort study, decreased BMI, HRT use after menopause, and alcohol consumption were
associated with an increased likelihood of IBC compared with SBC. The lower likelihood of IBC as a
breast density category increased and the different associations observed between a family history
of breast cancer and IBC by diagnostic period might reflect the wide application of breast
ultrasonography for breast cancer screening. Overall mortality of IBC was comparable with that of
SBC, but total and cancer-related mortality of IBC diagnosed between 6 and 12 months was higher
than that of SBC.
ARTICLE INFORMATION
Accepted for Publication: March 17, 2024.
Published: May 20, 2024. doi:10.1001/jamanetworkopen.2024.11927
Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2024 Song H
et al. JAMA Network Open.

Corresponding Author: Boyoung Park, MD, PhD, Department of Preventive Medicine, Hanyang University College
of Medicine, 222 Wangsimni-ro, Seongdong-gu, Seoul 04763, Republic of Korea (hayejine@hanyang.ac.kr).
Author Affiliations: Department of Preventive Medicine, Hanyang University College of Medicine, Seoul, Republic
of Korea (Song, Tran, Park); Biomedical Research Institute, Seoul National University Hospital, Seoul, Republic of
Korea (Kim); Hanyang Institute of Bioscience and Biotechnology, Hanyang University, Seoul, Republic of
Korea (Park).
Author Contributions: Dr Park had full access to all of the data in the study and takes responsibility for the
integrity of the data and the accuracy of the data analysis.
Concept and design: Song, Kim, Park.
Acquisition, analysis, or interpretation of data: Song, Tran, Park.
Drafting of the manuscript: Song, Park.
Critical review of the manuscript for important intellectual content: All authors.
Statistical analysis: Song, Tran.
Obtained funding: Park.
Administrative, technical, or material support: Kim.
Supervision: Kim, Park.
Conflict of Interest Disclosures: None reported.
Funding/Support: This work was supported by grant 2021R1A2C1011958 from the National Research Foundation
of Korea, funded by the Korean Ministry of Science and Information and Communication Technology.
Role of the Funder/Sponsor: The funder had no role in the design and conduct of the study; collection,
management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and
decision to submit the manuscript for publication.
Data Sharing Statement: See Supplement 2.
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SUPPLEMENT 1.
eTable 1. Factors Associated With Interval Breast Cancers Compared to Screen-Detected Breast Cancers According
to Breast Density
eTable 2. Factors Associated With Interval Breast Cancers Diagnosed Between 6 and 12 Months After Screening
Compared to Screening-Detected Breast Cancer According to Breast Density
eTable 3. Factors Associated With Interval Breast Cancers Diagnosed Between 12 and 24 Months Compared to
Screening-Detected Breast Cancers According to Breast Density
SUPPLEMENT 2.
Data Sharing Statement

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Original Investigation | Oncology

Abstract Key Points

JAMA Network Open. 2024;7(5):e2411927. doi:10.1001/jamanetworkopen.2024.11927

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Study Design and Population

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Definition of IBC and SBC

Established Risk Factors for Breast Cancer Considered in This Study

Figure. Study Flow Diagram

7 447 115 Women received mammographic breast

674 304 Excluded

6 772 811 Participants included in the analysis

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Table 1. Characteristics of the IBC and SBC Groupsa

Cancer type IBC diagnostic periodb

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Table 1. Characteristics of the IBC and SBC Groupsa (continued)

Cancer type IBC diagnostic periodb

Risk Factors for IBC vs SBC

Mortality Risk Among Women With IBC vs SBC

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Table 2. Risk Factors for IBC vs SBC

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Table 3. Mortality Among Women With IBC vs SBC

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Strengths and Limitations

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