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yankaskas-et-al-2012-association-of-recall-rates-with-sensitivity-and-positive-predictive-values-of-screening
yankaskas-et-al-2012-association-of-recall-rates-with-sensitivity-and-positive-predictive-values-of-screening
yankaskas-et-al-2012-association-of-recall-rates-with-sensitivity-and-positive-predictive-values-of-screening
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have been published previously [15, 16]. The Caro- true-positive study was a positive mammographic mammograms obtained in 155,289 women
lina Mammography Registry collects prospective examination that showed invasive breast cancer or were included for study. The mean age of this
mammography data from mammography facilities ductal carcinoma in situ that was diagnosed within population was 56 years; two thirds of the
and links these data to a breast pathology database 12 months of the screening examination. A true- screening mammograms were obtained in
that includes benign and malignant breast pathology negative study was a negative mammographic ex- women younger than 60 years. These women
records collected in an ongoing process from the pa- amination that did not show invasive breast cancer were 82.5% white, 16.2% black, and 1.3%
thology facilities themselves, from the North Caro- or ductal carcinoma in situ diagnosed within 12
“other.” Of all screening mammograms,
lina Central Cancer Registry, and from hospital and months of the examination. A false-negative study
13,552 led to a recommendation for further
private pathology departments. was a negative mammographic examination that
The study group included all screening mam- resulted in a breast cancer diagnosis within 12 workup—an overall recall rate of 6.3%. Recall
mography examinations for women living in North months of the study. A false-positive study was a rates and associated sensitivity, PPV, and can-
Carolina who underwent screening mammography positive mammographic examination that resulted cer detection rate are shown by demographics
in any participating facility between January 1994 in no diagnosis of cancer within 12 months. and breast history in Table 1. The highest re-
and June 1998. We identified all standard two-view Sensitivity was defined as the proportion of can- call rate (13.6%) among all the subgroups was
bilateral mammography examinations in the regis- cers that had positive mammographic findings seen in women who reported a breast problem
try, then selected those that were performed as within 12 months before the cancer diagnosis date, at screening; the lowest (2.4%) was in women
screening studies and excluded those that were diag- calculated as true-positive / (true-positive + false- with breasts categorized as almost entirely fat.
nostic studies. Mammography was considered a negative). The PPV for recall was defined as the pro-
The distribution of recommended follow-up
screening study if the patient was classified as as- portion of positive mammograms for which cancer
was diagnosed within 12 months of the screening,
visits was 68%, further imaging follow-up;
ymptomatic by the radiologist, the examination was
bilateral, and the examination was conducted at least calculated as true-positive / (true-positive + false- 16%, biopsy or surgical consultation; and
9 months after previous mammography. positive). Practice volume was calculated as the 0.5%, clinical follow-up. Fifteen percent of the
The mammography database contains data col- mean number of screening mammographic exami- recall follow-ups were missing the specific
lected from all patients at the time their mammography nations performed at the facility per year. For most recommendation for follow-up (not shown in
is performed, including demographic information, his- analyses, a missing response for family history of table). The 1-year cancer detection rate was
tory of breast procedures, reason for visit, hormone early breast cancer or personal history of breast can- 3.5 per 1000 mammograms obtained.
use, and family history of breast cancer (defined as a cer was classified as a negative response. The “can- In this population, recall rates decreased with
first-degree relative with premenopausal breast can- cer detection rate” was defined as the number of
increasing age, from 7.3% in women younger
cer). At each visit, the technologist and radiologist cancers discovered through mammography per 1000
than 50 years old to 4.9% in women 70 years
record information about the type of examination per- women screened. Sensitivity, PPV, cancer detection
rates, and recall rates were calculated for each prac- old and older. Women with a history of breast
formed (screening, diagnostic, sonography, or other di-
agnostic imaging modalities), comparison with tice. cancer were recalled at a greater rate than
previous films, density of breast parenchyma, mam- Reduced monotonic regression analysis [18] was women whose mammograms were negative for
mographic impression using the American College of used to model PPV and sensitivity rates as functions breast cancer: 7.4% and 6.3%, respectively. For
Radiology Breast Imaging Reporting and Data System of the recall rate for each of 31 radiology practices women who had a history of breast surgery or
(BI-RADS) [17] and recommendations for type of fol- included in the study. Reduced monotonic regres- breast procedures, the recall rate was 7.2%,
low-up study and follow-up time. Recommendations sion is a nonparametric approach based on the iso- compared with 6.3% for women who did not
for follow-up care may include additional mammogra- tonic regression theory. The reduced monotonic have this history. The recall rate decreased with
phy at specified intervals (immediately, 6 months, or 1 regression method simplifies the isotonic fit, identi-
decreasing breast density, from nearly 7.0% in
year), additional mammographic images, breast imag- fying cut points from an isotonic regression fit, re-
flecting locations in the recall rate at which the trend
the extremely dense and heterogeneously dense
ing using another modality, biopsy, or surgical consul-
tation. The number of mammograms obtained in the dependent variable (sensitivity or PPV) is groups to 2.4% in the almost entirely fat group.
annually at each facility can be calculated from data in most manifest. To avoid identifying a cut point be- Recall rates increased as elapsed time since pre-
the Carolina Mammography Registry database. tween two practices with nearly identical recall rates, vious mammogram increased: 5.2% in women
Outcome data from the pathology database in- practices whose recall rates differed by less than 1% having recent previous mammography versus
clude date and type of pathology, method of bi- of the range (i.e., by 0.12% in recall rate) were auto- 8.7% in women whose previous mammography
opsy, date of biopsy, breast site, number of nodes matically grouped together. For all analyses, the data was more than 36 months previous or who had
tested and number positive, estrogen and proges- for each practice are weighted by the number of no previous mammography.
terone receptor status, and tumor grade and stage. mammograms interpreted.
The largest difference was found between
All data are reviewed for quality. Detected errors Linear regression analysis was performed to ex-
women who reported symptoms at the time of
are corrected before the data are entered into the amine the association of recall rates with sensitiv-
registry. This project has the approval of the inter- ity and with PPV and to adjust for relevant their screening mammogram and those who did
nal review board of the Medical School of the Uni- covariates. In a second linear regression analysis, not report symptoms: 13.6% for women report-
versity of North Carolina at Chapel Hill and holds the recall rates were put into the models according ing symptoms, which was twice the 6.1% for
a certificate of confidentiality from the United to the groupings that resulted from the reduced women not reporting symptoms. Recall rates
States Public Health Service. monotonic regression. were greater in black women than in white and
3 2,172 2,862 3.6 62.5 4.8 1.7 to the data and provides an estimate of how sen-
4 18,186 28,053 3.8 63.7 7.3 2.8 sitivity increases with increasing recall rate. Fig-
ure 2 shows the analogous results for the
5 17,127 21,415 4.4 67.6 7.3 3.2
relationship of PPV as a function of recall rate,
6 812 814 4.9 100 2.5 1.2
where PPV declines with increasing recall rate.
7 897 909 5.2 0.0 0.0 0.0
The reduced monotonic regression shows that
8 4,743 6,230 5.2 76.5 8.0 4.2 the trends for both sensitivity and PPV are sta-
9 1,310 1,310 5.5 77.8 9.7 5.3 tistically significant. (Reduced monotonic re-
10 627 634 5.8 50.0 16.2 9.5 gression models the outcome variable as a
11 7,867 11,284 5.9 65.2 4.5 2.7 constant within groups defined by cut points.)
12 33,485 47,338 5.9 83.9 5.6 3.3 For sensitivity, a single cut point was identified
13 1,460 1,743 6.2 75.0 2.8 1.7 at a recall rate of 4.6% ( p < 0.0001). A cut point
for the relationship between recall rate and PPV
14 4,163 4,368 6.4 72.2 4.7 3.0
was identified at a recall rate of 8.8% ( p <
15 921 926 6.4 100 6.8 4.3
0.001). A second suggestive, although statisti-
16 4,282 5,205 6.5 72.7 7.1 4.6
cally not significant, cut point for PPV ( p =
17 3,133 4,497 7.0 77.8 6.6 4.7 0.13) was obtained at a recall rate of 5.7%. For
18 7,404 8,100 7.2 78.0 5.5 4.0 practices with recall rates between 1.9 and
19 19,608 35,122 7.2 82.7 6.6 4.8 4.4%, the average sensitivity was 65%; for the
20 1,984 2,149 7.5 80.0 5.0 3.7 remaining practices with recall rates greater
21 1,100 1,417 7.6 80.0 3.7 2.8 than 4.4%, the average sensitivity was 80% (Ta-
22 906 1,330 8.3 90.0 8.1 6.8 ble 4). The average PPV was 7.2% for practices
with recall rates of 1.9–5.5%, 5.9% for practices
23 695 782 8.6 75.0 4.5 3.8
with recall rates of 5.8–8.7%, and 3.3% for
24 833 848 8.7 80.0 5.4 4.7
practices with recall rates of 8.9% or greater.
25 1,963 2,692 8.9 83.3 2.1 1.9
Linear regression analysis was first per-
26 5,199 8,360 8.9 78.6 3.0 2.6 formed for recall as a continuous variable con-
27 2,374 2,945 9.5 84.6 3.9 3.7 trolling for the covariates of age, race, family
28 898 907 9.8 0.0 0.0 0.0 and personal history of breast cancer, history of
29 4,124 4,955 9.8 75.0 4.9 4.8 breast surgery or biopsy, presence of symptoms,
30 4,496 5,448 12.0 87.5 3.2 3.9 and breast density. The analysis showed that
31 1,328 1,353 13.4 75.0 3.3 4.4 practices with greater recall rates have greater
sensitivity ( p = 0.003, r 2 = 0.64). When the re-
Note.—Reported values of zero indicate no cancers occurred for that practice during the study period. PPV = positive pre-
dictive value. duced monotonic regression cut point of 4.6%
a Number detected per 1000 mammographic examinations performed. was used for the recall rate, the fit improved to
r 2 = 0.68. Linear regression analysis likewise
sociation of the recall rate with the PPV was 1000. The cancer detection rates are displayed showed that PPV decreased as recall rate in-
seen for racial group or family history of breast in the last column of Table 1. The largest differ- creased ( p = 0.0002), with an overall r 2 of 0.56.
cancer, although the PPV was greater in women ence in recall rate and associated cancer detec- When the practices are split into groups based
with a family history of breast cancer (Table 1). tion was seen for the presence of symptoms at on the reduced monotonic regression cut points,
Looking at practice volume, we found an in- screening. Recall rates rose from 6.1% in the model fit improved to 0.66.
verse relationship of PPV to recall rate for mean women who did not have symptoms to 13.6%
practice volume, with PPV increasing from 4.4% in symptomatic women, with the associated
in practices with the lowest volume to 6.4% in cancer detection rate rising from 3.4 to 10.3 per Discussion
practices with the largest volume, and recall rates 1000. No association between recall rate and The main purpose of this study was to ex-
decreased from 8.3% to 5.6% (Table 2). cancer detection was seen with respect to race, amine the association of recall rates with
family history of breast cancer, or breast density. sensitivity and PPV. We found no published
Recall Rate and Cancer Detection Rate study that focuses on recall rates alone. A
The overall cancer detection rate (cancers Recall Rate, Sensitivity, and PPV search using the terms “recall rates” and
seen on screening mammograms as a percent- The individual data for each practice in the “performance” turned up studies that men-
age of the total screened population) was 3.5 per study are displayed in Table 3. The recall rates tioned recall rates in the pursuit of measuring
our population are similar to the population creased, and PPV decreased. Black women Netherlands: results of initial and subsequent screen-
distribution for North Carolina in their age and had greater recall rates and lower PPVs than ing 1990-1995. Int J Cancer 1998;75:694–698
6. Kollias J, Sibbering DM, Blamey RW, et al.
racial distribution except for underrepresenta- white women. The percentage of women
Screening women aged less than 50 years with a
tion of older black women, in keeping with the with longer than 36 months from the previ- family history of breast cancer. Eur J Cancer
lower screening rates for these women in gen- ous screening or with no previous screening 1998;34:878–883
eral, not just in North Carolina [34, 35]. As was also greater for black women than for 7. Kerlikowske K, Grady D, Barclay J, Sickles EA,
others have reported, we found that recall rates white women. This trend of recall and PPV Ernster V. Effect of age, breast density, and fam-
ily history on the sensitivity of first screening
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were higher for women who were younger; with increasing elapsed time since screening
were black; had a history of breast biopsy, may explain the different findings in black mammography. JAMA 1996;276:33–38
8. Slanetz PJ, Giardino AA, McCarthy KA, et al.
breast surgery, or breast cancer; or had higher and white women.
Previous breast biopsy for benign disease rarely
breast density [7, 9, 36]. We also found that re- No reports exist of the association of recall complicates or alters interpretation on screening
call rates were greater for the presence of re- with both PPV and sensitivity to compare with mammography. AJR 1998;170:1539–1541
ported symptoms at screening and longer time our results. When grouping practices by vol- 9. Stomper PC, D’Souza DJ, DiNitto PA,
elapsed since the previous screening. We ume, we found that an increase in mean vol- Arredondo MA. Analysis of parenchymal density
found recall rates for women with and those ume of mammograms was associated with a on mammograms in 1353 women 25–79 years
old. AJR 1996;167:1261–1265
without a family history of breast cancer to be decrease in recall rate for screening volumes of
10. Warren RML, Duffy SW. Comparison of single
virtually the same. more than 200 per month with no difference in reading with double reading of mammograms,
In our data, for the most part, recall rates strat- sensitivity and an increase in PPV. and change in effectiveness with experience. Br J
ified within the covariates of interest showed an The key question we posed in this study Radiol 1995;68:958–962
association with sensitivity. As age increased, re- was whether a point existed at which sensitiv- 11. Seguret F, Daures JP, Guizard AV, et al. Herault
call rates decreased and sensitivity increased. ity reached a plateau as the recall rate in- breast screening programme: results after 30
months of a mobile French schedule. Eur J Can-
Recall rates increased and sensitivity decreased creased, while PPV continued to decline. We
cer Prev 1995;4:299–305
with increasing breast density when there was a did not find previous reports addressing this 12. Blanks RG, Wallis RM, Given-Wilson RM. Ob-
history of breast (or other) cancer, previous question. Our regression analyses showed that server variability in cancer detection during rou-
breast surgery, or biopsy; or when symptoms practices with recall rates of 4.4% or less had tine repeat (incident) mammographic screening
were reported at screening. Only with an in- lower sensitivity than the remaining practices, in a study of two versus one view mammography.
crease in time elapsed since the last screening which had recall rates of 4.8% or greater. J Med Screen 1999;6:152–158
did recall rates and sensitivity both increase. However, no statistically significant increase in 13. Perry NM, Kirkpatrick A. European guidelines
for quality assurance in mammography screen-
For the association of recall rates with PPV, sensitivity was noted among the practices once
ing. In: de Wolf CJM, Perry NM, eds. European
we found that women in the oldest age group a recall rate of 4.8% was reached. Although we guidelines for quality assurance in mammogra-
(≥ 70 years) had a recall rate of 4.9% with a must be cautious not to overinterpret the loca- phy screening, 2nd ed. Luxembourg: Office for
PPV of 12.7%, and women 60–69 years old tion of the cut point, both Figure 1 and Table 4 Official Publications of the European Communi-
had a recall rate of 5.8% with a PPV of 8.2%. clearly show that, for these data, the sensitivity ties, 1996:I-1–I-15
Welch and Fisher [22] studied recall from increased very little, if at all, beyond a recall 14. Quality Determinants of Mammography Guide-
line Panel. Quality determinants of mammogra-
Medicare claims data in women 65 and older rate of 4.8%. Conversely, a decline in PPV was
phy. Rockville, MD: United States Department of
and reported a recall rate of 8.5% and a PPV of observed with increasing recall rates for prac- Health and Human Services, Public Health Ser-
8% for women having further testing within 8 tices with recall rates of 8.9% or greater, and to vice, Agency for Health Care Policy and Re-
months of screening. We would have expected a lesser extent for practices with recall rates of search, 1994:78–86
this PPV to be higher because it was based on 5.9–8.7% (Fig. 2). Combining these findings, 15. Yankaskas BC, Jones MB, Aldrich TE. The Caro-
women who were actually followed up for fur- we conclude that practices with recall rates be- lina Mammography Registry: a population-based
ther workup, whereas ours is based on those tween 4.9% and 5.5% achieve the best trade- mammography and cancer surveillance project. J
Registry Manage 1996;23:175–178
for whom further workup was only recom- off of sensitivity and PPV.
16. Ballard-Barbash R, Taplin SH, Yankaskas BC, et
mended. Our findings for the relationship be- al. Breast Cancer Surveillance Consortium: a na-
tween recall and history of biopsy or surgery tional mammography screening and outcomes
are the same as those reported by Slanetz et al. References database. AJR 1997;169:1001–1008
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