IJC International Journal of Cancer
Overdiagnosis by mammographic screening for breast cancer studied in birth cohorts in The Netherlands T.M. Ripping1, A.L.M. Verbeek1,2, J. Fracheboud3, H.J. de Koning3, N.T. van Ravesteyn3 and M.J.M. Broeders1,2 1
Department for Health Evidence, Radboud university medical center, Nijmegen, The Netherlands Dutch Reference Center for Screening, Nijmegen, The Netherlands 3 Department of Public Health, Erasmus MC, University Medical Center Rotterdam, The Netherlands 2
Mammographic screening reduces breast cancer mortality1 by detecting breast cancers at an early stage with better treatment outcomes.2 A drawback of early detection by mammographic screening is, however, the detection of rather indolent breast cancers that would never have become clinically diagnosed during a woman’s lifetime. These indolent cancers are, so-called, “overdiagnosed.” Overdiagnosis is especially harmful when treatment follows, which is referred to as overtreatment. To date, there is much debate about the degree of overdiagnosis with estimates ranging from 0 to 52%.3–8 The major reason for this wide range of overdiagnosis estimates is the difficulty in quantifying the true extent of overdiagnosis, because studies with ideal empirical data and follow up until death do not exist1,5 and because there is no consensus about the optimal methodology to quantify overdiagnosis. H.J. Koning is member Research Oversight Committee Genome Canada. DOI: 10.1002/ijc.29452 History: Received 2 Dec 2014; Accepted 13 Jan 2015; Online 22 Jan 2015 Correspondence to: T.M. (Dorien) Ripping, Department for Health Evidence, Radboud university medical center, PO Box 9101, 6500 HB Nijmegen, The Netherlands, Fax: 1[31-24-361-3505], E-mail: [email protected]
C 2015 UICC Int. J. Cancer: 137, 921–929 (2015) V
Ideally, overdiagnosis is estimated from the breast cancer incidence in a screened and unscreened cohort of women using the cumulative-incidence approach,1,9,10 also called excess-incidence approach.11,12 For a valid comparison of the screened and unscreened cohort, the cohorts should have the same age distribution and risk of breast cancer,1 and there should be no contamination in the screened and unscreened group of women.9,13 Furthermore, the follow-up after the upper age-limit of the mammographic screening program should be at least 10-years to adjust for lead time,14 but preferably longer.1,15 Unfortunately, there are no cohort studies fulfilling all of these criteria. An age-period-cohort (APC) model with variables for the different phases of screening is a good secondary approach as was suggested by Puliti et al.13 Until now, such an APC-model has been used only once to estimate overdiagnosis at a period in time.6,16 Overdiagnosis estimates at a period in time have, however, as major disadvantage that they do not study the increase in breast cancer incidence during screening and the drop in incidence after leaving screening in the same women thereby overestimating overdiagnosis.17 This disadvantage can be overcome by studying overdiagnosis in birth cohorts, i.e., following the same women over time. Therefore, the aim of this study is to quantify overdiagnosis of the Dutch mammographic screening program in birth cohorts using an
Epidemiology
A drawback of early detection of breast cancer through mammographic screening is the diagnosis of breast cancers that would never have become clinically detected. This phenomenon, called overdiagnosis, is ideally quantified from the breast cancer incidence of screened and unscreened cohorts of women with follow-up until death. Such cohorts do not exist, requiring other methods to estimate overdiagnosis. We are the first to quantify overdiagnosis from invasive breast cancer and ductal carcinoma in situ (DCIS) in birth cohorts using an age-period-cohort -model (APC-model) including variables for the initial and subsequent screening rounds and a 5-year period after leaving screening. Data on the female population and breast cancer incidence were obtained from Statistics Netherlands, “Stichting Medische registratie” and the Dutch Cancer Registry for women aged 0–99 years. Data on screening participation was obtained from the five regional screening organizations. Overdiagnosis was calculated from the excess breast cancer incidence in the screened group divided by the breast cancer incidence in presence of screening for women aged 20–99 years (population perspective) and for women in the screened-age range (individual perspective). Overdiagnosis of invasive breast cancer was 11% from the population perspective and 17% from the invited women perspective in birth cohorts screened from age 49 to 74. For invasive breast cancer and DCIS together, overdiagnosis was 14% from population perspective and 22% from invited women perspective. A major strength of an APC-model including the different phases of screening is that it allows to estimate overdiagnosis in birth cohorts, thereby preventing overestimation.
922
Overdiagnosis in birth cohorts
What’s new? The extent of overdiagnosis of breast cancer associated with screening by mammography remains uncertain. The absence of ideal study cohorts is to blame, but an optimal quantitative secondary approach has also been lacking. Here, overdiagnosis was quantified from mammographic screening data in birth cohorts using an age-period-cohort model that included variables for multiple rounds of screening. The approach allowed the same women to be followed over time, thereby eliminating the possibility of overestimation. With the model, the estimated combined overdiagnosis of invasive breast cancer and ductal carcinoma in situ was found to range from 14% to 22%.
APC-model including variables representing the initial round, subsequent rounds and a 5-year period after leaving screening.
Material and Methods Setting
From 1989 to 1996, the mammographic screening program was implemented in The Netherlands, inviting women aged 50–69 years biennially. From 1997 onwards, women aged 70–74 years were invited also, with the program reaching full coverage in 2001. In 2004–2010, screen-film mammography was replaced by digital mammography.18 The mammographic screening program in The Netherlands has always had high attendance rates, ranging from 72% in 1990 to about 80% from 1997 onwards, and low percentages of definite nonparticipants (2.0–7.5%), consisting of women who do not wish to receive any further invitations to screening. Recall rates were 0.8% in the starting period and increased to 2.3% nowadays. Women receive an invitation for a subsequent screening exam on average 2 years after their screening exam. A small percentage (4.5%) of women has a screening interval longer than 2.5 years.18
Epidemiology
Breast cancer incidence data
Stichting Medische Registratie provided data on the number of invasive breast cancer incident cases for the period 1975– 1988. The website of the National Cancer Registry in The Netherlands19 provided data on the number of invasive breast cancer cases and ductal carcinoma in situ (DCIS) cases for the period 1989–2009. Statistics Netherlands20 provided data on the number of females aged 0–99 years living in The Netherlands per calendar year (1950–2009) in 5-year age groups. Because birth cohorts were calculated from 5-year age and period groups, each birth cohort consists of nine overlapping years indicated by the middle 5-years. Table 1 presents the absolute number of invasive breast cancer incidence, total breast cancer incidence and person-years by birth cohort and age. Screening participation
The number of women attending the mammographic screening program after their initial and subsequent invitation was collected centrally from the screening organizations and cate-
gorized per calendar year in 5-year age groups. The proportion of women having their initial (SCREEN1) and subsequent screen (SCREEN2) was calculated as the number of women attending screening divided by the number of women-years. In order to calculate the proportion of women leaving the screening program after 0–5 years (SCREEN3), we assumed that only women above age 75 left the program, except for the period 1995–1999 when women aged 70–74 years temporarily also left the screening program. We further assumed the proportion of women that died from all causes between the ages 65–94 was independent of screening. The proportions of SCREEN3 were calculated by subtracting the proportion of women attending screening at age 70–74, 75–79 or 80–84 from the proportion of women attending screening at age 65–69, 70–74 or 75–79, respectively. For example, the proportion of women leaving screening after 0–5 years (SCREEN3) was 13.6 for the age group 75–79 in the birth cohort 1923– 1927. This was calculated by subtracting the proportion of women in this age groups that still attended screening (i.e., SCREEN2 at age 75–79, which was 0.7) from the total proportion of women that were screened at age 70–74 (i.e., SCREEN1 and SCREEN2 at age 70–74, which were 2.5 and 11.8, respectively). Because the usual screening interval is two years in The Netherlands, all proportions were multiplied by two (Table 2). Statistical analysis
Statistical analyses were carried out with SAS (version 9.2). Negative binomial regression analysis was used to model first the invasive breast cancer incidence and second the invasive breast cancer plus DCIS incidence between 1975 and 2009 in women aged 20–99 years. The logarithm of the incidence rate is described as: Log IRRapc 5f ðaÞ 1 gðcÞ 1 hðpÞ 1S1 p1 1S2 SCREEN2 1S3 SCREEN3
(1)
In this regression formula, IRRapc is the relative (invasive) breast cancer incidence rate in age group a, cohort c and period p, f(a) are the age-specific rates, g(c) is the cohort component of cohort c and h(p) is the period component of period p.21–23 S1, S2 and S3 are the coefficients for the screening variables SCREEN1, SCREEN2 and SCREEN3, respectively.24 Goodness of fit was evaluated by comparing the deviance (dev) with the degrees of freedom (df) of the model C 2015 UICC Int. J. Cancer: 137, 921–929 (2015) V
45–49
50–54
55–59
60–64
65–69
70–74
75–79
80–84
C 2015 UICC Int. J. Cancer: 137, 921–929 (2015) V
35
38
33
38
56
1963–1967
1968–1972
1973–1977
1978–1982
1983–1987
7,918
6,102
4,055
1,725
1943–1947
Epidemiology
2,977
2,507
1938–1942
5,154
3,461
7,662
5,297
3,477
3,344
2,247 1,338
1933–1937
3,397
1928–1932
8,083
5,815
5,075
3,676
9,055
6,758
6,014
5,577
4,286
3,849
3,580 3,363
1923–1927
3,910
7,773
6,389
5,877
6,317
4,233
6,867
6,579
5,364
4,717
4,016
3,756
3,533 3,574
1918–1922
3,714
1908–1912
1913–1917
3,207 3,444
1903–1907
3,968
4,577
4,957
4,194
3,429
4,244
4,062
3,523
3,226
2,524
3,081
8,226
7,760
7,173
6,841
5,688
3,663
4,290
1,556
4,479
7,267
6,364
7,920
6,745
6,027
5,328
5,883
4,990
3,904
3,376
2,013
2,278
2,307
4,344
3,619
5,899
4,773
5,160
4,650
5,303
5,890
4,720
4,048
2,629
692
916
974
932
2,006
1,860
3,529
2,977
4,785
3,477
5,162
4,286
4,523
4,016
3,106
2,524
1898–1902
263
242
254
258
951
1,747
3,461
3,676
4,233
3,429
1893–1897
Invasive plus DCIS
53
1958–1962
820
218
48
1953–1957
214
871
1948–1952
1,725
692
216
1943–1947
2,507
1938–1942
3,344
2,247 1,338
1933–1937
3,397
1928–1932
3,849
3,580 3,363
1923–1927
3,910
3,756
3,533 3,574
1918–1922
3,714
1908–1912
1913–1917
3,207 3,444
1903–1907
3,081
40–44
1,556
35–39
2,013
30–34
2,629
25–29
1898–1902
20–24
1893–1897
Invasive
Cohort
Age
Table 1. Absolute number of invasive breast cancers, invasive breast cancers plus DCIS and person-years by cohort and age
2,713
2,410
1,894
1,674
2,628
2,327
1,805
1,621
85–89
1,000
779
636
511
972
764
616
503
90–94
159
109
109
67
155
105
108
64
95–99
Ripping et al.
923
35
40
34
41
60
1963–1967
1968–1972
1973–1977
1978–1982
1983–1987
4,881
4,650
3,925
45–49
7,997
6,908
6,407
50–54
9,647
9,108
55–59 8,963
60–64
65–69
70–74
75–79
85–89
90–94
95–99
549770.5 324981.5138853.538625.5
80–84
1,878,5031,839,9351,780,5171,694,3961561450.51,361,8271,082,226
173,7803 1,680,9581,596,7351,472,357 1,280,195997606.5 647609.5
1,574,9801,491,3321368710.51,185,994915,934 570,076 255,135
1,452,6961324656.51,138,148873069.5 540868.5230,410 65673.5
2,826,9652,868,9802,875,1552,892,9102,893,8892,879,0202,830,611
3,026,6093,058,1483,094,9283,113,2303,120,4493,087,135
3,110,1143,177,9363,214,5373,243,6183,220,191
3,037,1523,107,2223,169,0283,155,002
2,523,2712,638,7032,657,901
2,392,3972,472,178
2,420,779
1958–1962
1963–1967
1968–1972
1973–1977
1978–1982
1983–1987
2,847,1872,857,9552,854,8062,860,2812,842,6872,806,1612,739,973
2,537,0952,541,7352,535,9772,526,1522,492,4332,442,3612,364,100
2,052,2422,058,1332,045,2562,024,6591,983,8701,924,6691,838,585
1,905,9861,897,8421,875,4001,840,1841,782,2071,699,5091582361.5
1,896,3731,873,9901,834,7191,777,7911,690,6081,561,504 1,379,064
1953–1957
1948–1952
1943–1947
1938–1942
1933–1937
1928–1932
1923–1927
1918–1922
1913–1917
1908–1912
1228072.51,039,811787,400 483912.5205,912 54,703
2,463
2,495
2,163
1,970
40–44 3,766
1903–1907
986
1,043
1,015
999
820
35–39 1,747
897,569 665340.5 404,368 172,893 46,357
285
253
272
271
30–34 871
1898–1902
1893–1897
Person-years
53
1958–1962
214
218
48
1953–1957
25–29
216
20–24
1948–1952
Cohort
Age
Table 1. Absolute number of invasive breast cancers, invasive breast cancers plus DCIS and person-years by cohort and age (Continued)
Epidemiology
924 Overdiagnosis in birth cohorts
C 2015 UICC Int. J. Cancer: 137, 921–929 (2015) V
925
Ripping et al.
Table 2. The percentage of women years attending (SCREEN1, SCREEN2) and leaving (SCREEN3) the mammographic screening program Age (a)
SCREEN1
SCREEN2
1918–1922
70–74
0.6
2.0
0.1
0.1
2.4
80–84
0.0
0.0
0.2
90–943 65–69 70–74
0.0
14.42 11.8
0.0 18.6
80–84
0.0
0.0
0.8
85–893
0.0
0.0
0.0
3
0.0
0.0
0.0
60–64
80–843
1948–1952
2.5
0.0
13.6
75–79
1943–1947
16.1
19.7 7.4 1.4 0.0 0.0
18.52 54.12 65.5 0.8
0.0
0.0
90–943
0.0
0.0
0.0 0.0 0.0
0.8
0.0 2
55–59
19.9
18.2
0.0
9.7
65.72
0.0
65–69
0.5
75.0
0.0
70–74
0.2
70.1
0.0
3
75–79
0.0
0.0
70.4
80–843
0.0
0.0
0.0
3
85–89
0.0
0.0
0.0
50–54
23.0
15.22 2
SCREEN1
SCREEN2
55–59
0.4
77.1
0.0
60–643
0.0
77.0
0.0
65–693
0.0
76.0
0.0
3
70–74
0.0
71.6
0.0
75–793
0.0
0.0
71.6
3
80–84
0.0
0.0
0.0
85–893
0.0
0.0
0.0
SCREEN3
45–49
15.7
0.0
0.0
50–54
16.0
60.4
0.0
55–593
0.0
76.8
0.0
60–643
0.0
76.3
0.0
3
65–69
0.0
75.2
0.0
70–743
0.0
70.9
0.0
3
75–79
0.0
0.0
70.9
80–843
0.0
0.0
0.0
3
0.0
0.0
0.0
1
No distinction was made between regular screening (interval
Overdiagnosis by mammographic screening for breast cancer studied in birth cohorts in The Netherlands T.M. Ripping1, A.L.M. Verbeek1,2, J. Fracheboud3, H.J. de Koning3, N.T. van Ravesteyn3 and M.J.M. Broeders1,2 1
Department for Health Evidence, Radboud university medical center, Nijmegen, The Netherlands Dutch Reference Center for Screening, Nijmegen, The Netherlands 3 Department of Public Health, Erasmus MC, University Medical Center Rotterdam, The Netherlands 2
Mammographic screening reduces breast cancer mortality1 by detecting breast cancers at an early stage with better treatment outcomes.2 A drawback of early detection by mammographic screening is, however, the detection of rather indolent breast cancers that would never have become clinically diagnosed during a woman’s lifetime. These indolent cancers are, so-called, “overdiagnosed.” Overdiagnosis is especially harmful when treatment follows, which is referred to as overtreatment. To date, there is much debate about the degree of overdiagnosis with estimates ranging from 0 to 52%.3–8 The major reason for this wide range of overdiagnosis estimates is the difficulty in quantifying the true extent of overdiagnosis, because studies with ideal empirical data and follow up until death do not exist1,5 and because there is no consensus about the optimal methodology to quantify overdiagnosis. H.J. Koning is member Research Oversight Committee Genome Canada. DOI: 10.1002/ijc.29452 History: Received 2 Dec 2014; Accepted 13 Jan 2015; Online 22 Jan 2015 Correspondence to: T.M. (Dorien) Ripping, Department for Health Evidence, Radboud university medical center, PO Box 9101, 6500 HB Nijmegen, The Netherlands, Fax: 1[31-24-361-3505], E-mail: [email protected]
C 2015 UICC Int. J. Cancer: 137, 921–929 (2015) V
Ideally, overdiagnosis is estimated from the breast cancer incidence in a screened and unscreened cohort of women using the cumulative-incidence approach,1,9,10 also called excess-incidence approach.11,12 For a valid comparison of the screened and unscreened cohort, the cohorts should have the same age distribution and risk of breast cancer,1 and there should be no contamination in the screened and unscreened group of women.9,13 Furthermore, the follow-up after the upper age-limit of the mammographic screening program should be at least 10-years to adjust for lead time,14 but preferably longer.1,15 Unfortunately, there are no cohort studies fulfilling all of these criteria. An age-period-cohort (APC) model with variables for the different phases of screening is a good secondary approach as was suggested by Puliti et al.13 Until now, such an APC-model has been used only once to estimate overdiagnosis at a period in time.6,16 Overdiagnosis estimates at a period in time have, however, as major disadvantage that they do not study the increase in breast cancer incidence during screening and the drop in incidence after leaving screening in the same women thereby overestimating overdiagnosis.17 This disadvantage can be overcome by studying overdiagnosis in birth cohorts, i.e., following the same women over time. Therefore, the aim of this study is to quantify overdiagnosis of the Dutch mammographic screening program in birth cohorts using an
Epidemiology
A drawback of early detection of breast cancer through mammographic screening is the diagnosis of breast cancers that would never have become clinically detected. This phenomenon, called overdiagnosis, is ideally quantified from the breast cancer incidence of screened and unscreened cohorts of women with follow-up until death. Such cohorts do not exist, requiring other methods to estimate overdiagnosis. We are the first to quantify overdiagnosis from invasive breast cancer and ductal carcinoma in situ (DCIS) in birth cohorts using an age-period-cohort -model (APC-model) including variables for the initial and subsequent screening rounds and a 5-year period after leaving screening. Data on the female population and breast cancer incidence were obtained from Statistics Netherlands, “Stichting Medische registratie” and the Dutch Cancer Registry for women aged 0–99 years. Data on screening participation was obtained from the five regional screening organizations. Overdiagnosis was calculated from the excess breast cancer incidence in the screened group divided by the breast cancer incidence in presence of screening for women aged 20–99 years (population perspective) and for women in the screened-age range (individual perspective). Overdiagnosis of invasive breast cancer was 11% from the population perspective and 17% from the invited women perspective in birth cohorts screened from age 49 to 74. For invasive breast cancer and DCIS together, overdiagnosis was 14% from population perspective and 22% from invited women perspective. A major strength of an APC-model including the different phases of screening is that it allows to estimate overdiagnosis in birth cohorts, thereby preventing overestimation.
922
Overdiagnosis in birth cohorts
What’s new? The extent of overdiagnosis of breast cancer associated with screening by mammography remains uncertain. The absence of ideal study cohorts is to blame, but an optimal quantitative secondary approach has also been lacking. Here, overdiagnosis was quantified from mammographic screening data in birth cohorts using an age-period-cohort model that included variables for multiple rounds of screening. The approach allowed the same women to be followed over time, thereby eliminating the possibility of overestimation. With the model, the estimated combined overdiagnosis of invasive breast cancer and ductal carcinoma in situ was found to range from 14% to 22%.
APC-model including variables representing the initial round, subsequent rounds and a 5-year period after leaving screening.
Material and Methods Setting
From 1989 to 1996, the mammographic screening program was implemented in The Netherlands, inviting women aged 50–69 years biennially. From 1997 onwards, women aged 70–74 years were invited also, with the program reaching full coverage in 2001. In 2004–2010, screen-film mammography was replaced by digital mammography.18 The mammographic screening program in The Netherlands has always had high attendance rates, ranging from 72% in 1990 to about 80% from 1997 onwards, and low percentages of definite nonparticipants (2.0–7.5%), consisting of women who do not wish to receive any further invitations to screening. Recall rates were 0.8% in the starting period and increased to 2.3% nowadays. Women receive an invitation for a subsequent screening exam on average 2 years after their screening exam. A small percentage (4.5%) of women has a screening interval longer than 2.5 years.18
Epidemiology
Breast cancer incidence data
Stichting Medische Registratie provided data on the number of invasive breast cancer incident cases for the period 1975– 1988. The website of the National Cancer Registry in The Netherlands19 provided data on the number of invasive breast cancer cases and ductal carcinoma in situ (DCIS) cases for the period 1989–2009. Statistics Netherlands20 provided data on the number of females aged 0–99 years living in The Netherlands per calendar year (1950–2009) in 5-year age groups. Because birth cohorts were calculated from 5-year age and period groups, each birth cohort consists of nine overlapping years indicated by the middle 5-years. Table 1 presents the absolute number of invasive breast cancer incidence, total breast cancer incidence and person-years by birth cohort and age. Screening participation
The number of women attending the mammographic screening program after their initial and subsequent invitation was collected centrally from the screening organizations and cate-
gorized per calendar year in 5-year age groups. The proportion of women having their initial (SCREEN1) and subsequent screen (SCREEN2) was calculated as the number of women attending screening divided by the number of women-years. In order to calculate the proportion of women leaving the screening program after 0–5 years (SCREEN3), we assumed that only women above age 75 left the program, except for the period 1995–1999 when women aged 70–74 years temporarily also left the screening program. We further assumed the proportion of women that died from all causes between the ages 65–94 was independent of screening. The proportions of SCREEN3 were calculated by subtracting the proportion of women attending screening at age 70–74, 75–79 or 80–84 from the proportion of women attending screening at age 65–69, 70–74 or 75–79, respectively. For example, the proportion of women leaving screening after 0–5 years (SCREEN3) was 13.6 for the age group 75–79 in the birth cohort 1923– 1927. This was calculated by subtracting the proportion of women in this age groups that still attended screening (i.e., SCREEN2 at age 75–79, which was 0.7) from the total proportion of women that were screened at age 70–74 (i.e., SCREEN1 and SCREEN2 at age 70–74, which were 2.5 and 11.8, respectively). Because the usual screening interval is two years in The Netherlands, all proportions were multiplied by two (Table 2). Statistical analysis
Statistical analyses were carried out with SAS (version 9.2). Negative binomial regression analysis was used to model first the invasive breast cancer incidence and second the invasive breast cancer plus DCIS incidence between 1975 and 2009 in women aged 20–99 years. The logarithm of the incidence rate is described as: Log IRRapc 5f ðaÞ 1 gðcÞ 1 hðpÞ 1S1 p1 1S2 SCREEN2 1S3 SCREEN3
(1)
In this regression formula, IRRapc is the relative (invasive) breast cancer incidence rate in age group a, cohort c and period p, f(a) are the age-specific rates, g(c) is the cohort component of cohort c and h(p) is the period component of period p.21–23 S1, S2 and S3 are the coefficients for the screening variables SCREEN1, SCREEN2 and SCREEN3, respectively.24 Goodness of fit was evaluated by comparing the deviance (dev) with the degrees of freedom (df) of the model C 2015 UICC Int. J. Cancer: 137, 921–929 (2015) V
45–49
50–54
55–59
60–64
65–69
70–74
75–79
80–84
C 2015 UICC Int. J. Cancer: 137, 921–929 (2015) V
35
38
33
38
56
1963–1967
1968–1972
1973–1977
1978–1982
1983–1987
7,918
6,102
4,055
1,725
1943–1947
Epidemiology
2,977
2,507
1938–1942
5,154
3,461
7,662
5,297
3,477
3,344
2,247 1,338
1933–1937
3,397
1928–1932
8,083
5,815
5,075
3,676
9,055
6,758
6,014
5,577
4,286
3,849
3,580 3,363
1923–1927
3,910
7,773
6,389
5,877
6,317
4,233
6,867
6,579
5,364
4,717
4,016
3,756
3,533 3,574
1918–1922
3,714
1908–1912
1913–1917
3,207 3,444
1903–1907
3,968
4,577
4,957
4,194
3,429
4,244
4,062
3,523
3,226
2,524
3,081
8,226
7,760
7,173
6,841
5,688
3,663
4,290
1,556
4,479
7,267
6,364
7,920
6,745
6,027
5,328
5,883
4,990
3,904
3,376
2,013
2,278
2,307
4,344
3,619
5,899
4,773
5,160
4,650
5,303
5,890
4,720
4,048
2,629
692
916
974
932
2,006
1,860
3,529
2,977
4,785
3,477
5,162
4,286
4,523
4,016
3,106
2,524
1898–1902
263
242
254
258
951
1,747
3,461
3,676
4,233
3,429
1893–1897
Invasive plus DCIS
53
1958–1962
820
218
48
1953–1957
214
871
1948–1952
1,725
692
216
1943–1947
2,507
1938–1942
3,344
2,247 1,338
1933–1937
3,397
1928–1932
3,849
3,580 3,363
1923–1927
3,910
3,756
3,533 3,574
1918–1922
3,714
1908–1912
1913–1917
3,207 3,444
1903–1907
3,081
40–44
1,556
35–39
2,013
30–34
2,629
25–29
1898–1902
20–24
1893–1897
Invasive
Cohort
Age
Table 1. Absolute number of invasive breast cancers, invasive breast cancers plus DCIS and person-years by cohort and age
2,713
2,410
1,894
1,674
2,628
2,327
1,805
1,621
85–89
1,000
779
636
511
972
764
616
503
90–94
159
109
109
67
155
105
108
64
95–99
Ripping et al.
923
35
40
34
41
60
1963–1967
1968–1972
1973–1977
1978–1982
1983–1987
4,881
4,650
3,925
45–49
7,997
6,908
6,407
50–54
9,647
9,108
55–59 8,963
60–64
65–69
70–74
75–79
85–89
90–94
95–99
549770.5 324981.5138853.538625.5
80–84
1,878,5031,839,9351,780,5171,694,3961561450.51,361,8271,082,226
173,7803 1,680,9581,596,7351,472,357 1,280,195997606.5 647609.5
1,574,9801,491,3321368710.51,185,994915,934 570,076 255,135
1,452,6961324656.51,138,148873069.5 540868.5230,410 65673.5
2,826,9652,868,9802,875,1552,892,9102,893,8892,879,0202,830,611
3,026,6093,058,1483,094,9283,113,2303,120,4493,087,135
3,110,1143,177,9363,214,5373,243,6183,220,191
3,037,1523,107,2223,169,0283,155,002
2,523,2712,638,7032,657,901
2,392,3972,472,178
2,420,779
1958–1962
1963–1967
1968–1972
1973–1977
1978–1982
1983–1987
2,847,1872,857,9552,854,8062,860,2812,842,6872,806,1612,739,973
2,537,0952,541,7352,535,9772,526,1522,492,4332,442,3612,364,100
2,052,2422,058,1332,045,2562,024,6591,983,8701,924,6691,838,585
1,905,9861,897,8421,875,4001,840,1841,782,2071,699,5091582361.5
1,896,3731,873,9901,834,7191,777,7911,690,6081,561,504 1,379,064
1953–1957
1948–1952
1943–1947
1938–1942
1933–1937
1928–1932
1923–1927
1918–1922
1913–1917
1908–1912
1228072.51,039,811787,400 483912.5205,912 54,703
2,463
2,495
2,163
1,970
40–44 3,766
1903–1907
986
1,043
1,015
999
820
35–39 1,747
897,569 665340.5 404,368 172,893 46,357
285
253
272
271
30–34 871
1898–1902
1893–1897
Person-years
53
1958–1962
214
218
48
1953–1957
25–29
216
20–24
1948–1952
Cohort
Age
Table 1. Absolute number of invasive breast cancers, invasive breast cancers plus DCIS and person-years by cohort and age (Continued)
Epidemiology
924 Overdiagnosis in birth cohorts
C 2015 UICC Int. J. Cancer: 137, 921–929 (2015) V
925
Ripping et al.
Table 2. The percentage of women years attending (SCREEN1, SCREEN2) and leaving (SCREEN3) the mammographic screening program Age (a)
SCREEN1
SCREEN2
1918–1922
70–74
0.6
2.0
0.1
0.1
2.4
80–84
0.0
0.0
0.2
90–943 65–69 70–74
0.0
14.42 11.8
0.0 18.6
80–84
0.0
0.0
0.8
85–893
0.0
0.0
0.0
3
0.0
0.0
0.0
60–64
80–843
1948–1952
2.5
0.0
13.6
75–79
1943–1947
16.1
19.7 7.4 1.4 0.0 0.0
18.52 54.12 65.5 0.8
0.0
0.0
90–943
0.0
0.0
0.0 0.0 0.0
0.8
0.0 2
55–59
19.9
18.2
0.0
9.7
65.72
0.0
65–69
0.5
75.0
0.0
70–74
0.2
70.1
0.0
3
75–79
0.0
0.0
70.4
80–843
0.0
0.0
0.0
3
85–89
0.0
0.0
0.0
50–54
23.0
15.22 2
SCREEN1
SCREEN2
55–59
0.4
77.1
0.0
60–643
0.0
77.0
0.0
65–693
0.0
76.0
0.0
3
70–74
0.0
71.6
0.0
75–793
0.0
0.0
71.6
3
80–84
0.0
0.0
0.0
85–893
0.0
0.0
0.0
SCREEN3
45–49
15.7
0.0
0.0
50–54
16.0
60.4
0.0
55–593
0.0
76.8
0.0
60–643
0.0
76.3
0.0
3
65–69
0.0
75.2
0.0
70–743
0.0
70.9
0.0
3
75–79
0.0
0.0
70.9
80–843
0.0
0.0
0.0
3
0.0
0.0
0.0
1
No distinction was made between regular screening (interval
