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Racial Differences in Timeliness of Follow-Up after
Abnormal Screening Mammography
Sophia W. Chang, M.D., M.P.H.’
Karla Kerlikowske, M.D?
Anna Napoles-Springer, M.P.H.’
Samuel F. Posner, P h n ’
Edward A. Sickles, M . D . ~
Eliseo J. Perez-Stable, M.D.’
Medical Effectiveness Research Center for Diverse Populations and Division of General Internal Medicine, Department of Medicine, University of California, San Francisco, California.
Department of Epidemiology and Biostatistics,
and General Internal Medicine Section, Department of Veterans Affairs, University of California, San Francisco, California.
Department of Radiology, University of California, San Francisco, California.
This work was supported by an AHCPR grant,
no. HS 07373 and NCI-funded Breast Cancer
SPORE grant, P50 CA58207. Dr. Kerlikowske is
supported, in part, by an American Cancer Society Career Development Award for Primary Care
A portion of this manuscript has been presented
in poster form at the 5th Annual Society for
General Internal Medicine Meeting, April 30,
1996, Washington, DC.
The authors thank Diane Emler, Cristina Amaya,
Stac:y Jones, John Barclay, and the staff of the
UCS8FMobile Mammography Program for their
help in collecting the information for our analyses. The authors also thank Anita Stewart for her
comments on earlier drafts of this manuscriDt.
Address for reprints: Sophia W. Chang, M.D.,
M.P.H., Medical Effectiveness Research Center
for Diverse Populations, University of California,
San Francisco, 3333 California St., Suite 300
M, San Francisco, CA 94143-0856.
Received March 7, 1996; revision received May
28, .1996; accepted May 28, 1996.
0 1996 American Cancer Society
BACKGROUND. To determine whether patient race was associated with timeliness
of follow-up after abnormal screening mammography, a retrospective record review of diagnostic tests for women with abnormal screening mammography from
a Northern California mobile van program was conducted.
METHODS. The study included 317 women between the ages of 33 and 85 who
were reported to have abnormal screening mammography between July 1993 and
May 1994. Measurements included patient demographics, screening mammography interpretation, follow-up diagnostic tests, and dates of diagnostic evaluation.
RESULTS. Women with abnormal screening mammography underwent a wide variety of diagnostic evaluations. Nonwhite women had significantly longer time (median time, 19 days) from date of index abnormal screening mammography to
final disposition compared with white women (median time, 12 days). This racial
difference was primarily due to the longer interval between index abnormal screening mammography and first diagnostic test (median time, 15 days for nonwhite
women versus 7 days for white women, P < 0.001). The difference persisted when
adjusting for patient age, family history of breast cancer, report of palpable mass,
and income. The racial difference was similarly significant for each nonwhite subgroup (African American, Latina, and Asian) when compared with white women
( P < 0.01).
CONCLUSIONS. Reasons for less timely follow-up of abnormal mammography
among nonwhite women need to be identified. Delays that may be instigated by
the patient or be due to her physician or system of care need to be explored
further. Cancer 1996;781395-1902. 0 1996 American Cancer Society.
KEYWORDS: breast neoplasms-diagnosis, mammography-prevention
trol, follow-up studies, time factors, ethnic groups.
and con-
reast cancer is the most common cancer diagnosed among all
women across all ethnic groups in the United States and is the
second leading cause of cancer death.’ Differences in breast cancer
mortality by race/ethnicity are striking, notably the higher mortality
rates for African-American women‘-5 despite higher incidence rates
among white, non-Hispanic (henceforth white) ~ o r n e n .The
~ ’ ~reasons for these mortality differences across race/ethnicities are not
completely understood. Studies have noted a strong correlation between mortality and socioeconomic tatu us,^" pointing to factors that
may affect mortality rates, e.g., access to health care and comorbid
conditions. Other studies have found that breast cancer tends to be
diagnosed at a later stage among African-American ~ o m e n , ~ fre’O
sulting in a higher breast cancer mortality rate.” There are also indications that tumor biology may differ by race, with African Americans
more likely to be estrogen and progesterone receptor negative and to
CANCER October 1, 1996 / Volume 78 / Number 7
have a high S-phase, both prognostic indicators of
more aggressive tumors and poorer survival.”
Within the past decade, increased rates of screening have been reported across all racial/ethnic
g r o ~ p s . ’ ~Recently
published data from the National
Cancer Institute show that there has been a decrease
in breast cancer mortality of 5.5% among white
women from 1989-1992 that may, in part, be due to
an increase in mammography utili~ation.~
There has
not, however, been a concomitant decrease in breast
cancer mortality among African-American women5
despite similar increased rates of mammography
screening.14It is unknown if there is differential followup after abnormal mammography screening among
racial/ethnic groups and, if differences exist, whether
this accounts for later breast cancer stage at diagnosis
and higher mortality rates.
Given that the diagnosis of breast cancer at an
early stage is generally accepted to be one of the most
important prognostic indicators for prolonged survival, the timeliness of evaluating abnormal screening
results becomes important. This study examined
whether raceiethnicity was a predictor of time to follow-up after abnormal screening mammography.
Subjects and Measurements
Data were abstracted from records of the University
of California at San Francisco (UCSF) Mobile Mammography Screening Program, which has performed
more than 78,000 screening examinations since 1985.
The program began recording patient race/ethnicity
in mid-July 1993. The program methodology and
definitions of database variables collected were wellalong with the screening chardescribed elsewhere,*’
acteristics of the population.18 In brief, the program
is an efficient, high-quality screening program with
mammographic interpretations performed by radiologists with specialized training in interpreting mammography.lgPatient breast cancer risk profile and clinical history were collected at the time of mammography screening via interview and entered directly into
a database. The information collected included age,
race/ethnicity, family history of breast cancer, report
of palpable mass, zip code, and referring provider.
Race/ethnicity was recorded based on staff ascertainment; when a staff member was unsure, race was
clarified by patient self-identification. Categories were
recorded as white, black, Hispanic, Chinese, Filipina,
Japanese, and other. Family history of breast cancer
was defined as having at least one first-degree relative
with breast cancer (mother, sister, daughter). The
presence of a palpable mass was based on personal
history or physical examination. As this study was a
retrospective review of patient records and there was
no direct participant contact with study investigators,
informed consent was not received per approval of the
institution’s committee on human subjects.
The database also included screening mammography interpretation with mammography read as normal
or abnormal. Abnormal mammography readings were
further classified according to the BI-RADS lexicon
categories adapted by the American College of Radiology‘”: (1) additional examinations needed; (2) suspicious for malignancy, biopsy recommended; and (3)
malignant by radiologic criteria, biopsy recommended. Separate interpretations were made for each
breast. For purposes of our analysis, the more abnormal reading was coded for women who have discordant interpretations between breasts. Results of subsequent diagnostic tests were also coded for each breast.
As part of the screening process, systematic follow-up
of patients with identified mammographic abnormalities was conducted using a computerized tracking sysOne month after an abnormal screening examination, a computer-generated letter requesting information about diagnostic procedures and clinical
outcome was mailed to the woman’s identified physician, unless follow-up information had already been
provided to the screening program. If physicians did
not respond to the mailed request within 1 month,
they were contacted by telephone. Standardized requests for follow-up information provided information
on the type, timing, and interpretation of subsequent
diagnostic tests as well as clinical outcome. Classification of breast cancer, if diagnosed, was based on the
American Joint Committee on Cancer staging system.”
Time to first diagnostic test was defined as the
number of days from index abnormal screening examination to first diagnostic test. Time to final disposition
was defined as the number of days from index abnormal screening examination to final disposition, i.e.,
cancer diagnosis or last diagnostic test that allowed
the physician to decide no further workup was necessary.
Data and Statistical Analysis
A total of seven women (2%)were missing the date of
their last diagnostic test. Three of these women were
white, and four were nonwhite. For these patients, the
overall sample’s median time to last diagnostic test
was used to calculate a final test date. This method
of imputation will generally underestimate any racial
differences in time to final diagnosis or disposition.
Income information (the only available socioeco-
Race Difference in Mammography Follow-UpKhang et al.
noinic status indicator) was operationalized in three
different ways using 1990 U S . Bureau of the Census
da1.a. First, patient income was estimated using the
median income of residence zip code. This method
has been commonly used to estimate income." To
test the impact of income further. a second indicator
(percentage of zip code area households with incomes
below poverty level) was also used." Income was also
dichotomized (as less than $20,000 annually vs.
$20,000 or more annually). Two women were missing
zip code/income matches and were therefore not included in the multivariate analyses described subsequently.
Comparisons of categorical demographic characteristics between white and nonwhite women were
tested for statistical significance using chi-square analysis. Continuous variables were compared between
groups using Student's t test or nonparametric (Wilcoxon rank-sum) methods in cases when measures
had nonnormal distributions.
Multivariate analyses were performed to determine significant predictors of time to diagnostic testing. The major dependent measures of time to diagnosis and time to first test were skewed to the right and
were therefore transformed using a natural log function to meet assumptions of normality. Two women
underwent same-day additional tests, and their time
to first test was set equal to 0.5 days to allow log transformation. Linear regression analysis was then performed to identify important predictors of log-transformed time to either first test or diagnosis/disposition. All analyses were performed using SAS for a
personal computer.
The variables included in the model were those
tlhat were available and that the authors presumed
would affect time to diagnostic follow-up. These variables include: age, raceIethnicity, family history of
breast cancer, presence of a palpable mass, income,
and screening mammography interpretation. In a recent review, older women have been shown to be more
likely to have longer time to diagnostic e~aluation.'~
Having a family history of breast cancer or a history
of a palpable mass might also affect the timing of diagnostic evaluation, with the likelihood of more aggressive (i.e., timely) follow-up. A suspicious or malignant
interpretation of the index screening mammography
was also included in the model, as it could similarly
act as an alert to the physician to pursue more timely
Final Study Group
.Among 6626 screening examinations performed between July 1993 and May 1994,337 were interpreted as
abnormal at the end of the study period. Twelve records
were not entered in our analytical database; 10 records
were missing, and 2 were pending final disposition.
Eight additional women were not included in the analysis. Four women had no documented follow-up as of
6 months after index abnormal mammography, two
were white women and two were Latinas (one of whom
reportedly refused additional tests). One woman had
missing raceIethnicity information, and three women
were excluded because they had a previous history of
breast cancer. Because women with a previous history
of breast cancer are eligible for mammography screening, a repeat analysis was conducted including these
women; their inclusion did not alter our study findings.
The final study sample, therefore, consisted of 317
women with an abnormal result of a screening mammography examination during the study period with
documented follow-up. In all, 95% of those eligible
were included in the analysis.
Baseline Characteristics
The mean age of the women studied was 52 years
(range, 33 to 85), with 48% of the sample aged 50 or
older. The majority of the sample was white (64%),
with 16% Latinas, 12% Asians, and 8%African Americans, which closely reflects the San Francisco Bay Area
population statistics of 64% whites, 11% Latinas, 17%
Asians, and 8%African Americans.25Fifty-four percent
were first-time mammography screeners, and 8%were
noted to have a palpable mass by history or physical
examination at the time of screening. Compared with
white women, nonwhite women (Table 1) were less
likely to have a family history of breast cancer, had
a lower median income, and were more likely to be
undergoing their first screening mammography.
Abnormal screening mammography interpretation did not differ significantly by race (Table 2). Median time to final disposition differed significantly ( P
< 0.001) by race, with medians of 12 days (range, 1 to
192) for white women and 19 days (range, 2 to 176)
for nonwhite women. Median time to first diagnostic
test also differed significantly ( P < 0.001) for white
versus nonwhite women at 7 days (range, 0 to 161)
and 15 days (range, 2 to 1261, respectively. The overall
difference in time to final disposition appears to be
explained by the lag time to first diagnostic test. That
is, the median times from first diagnostic test to final
disposition did not differ significantly ( P = 0.06) between white and nonwhite women.
Among women evaluated for abnormal mammography, 30 were diagnosed with breast cancer. Ten
cases were ductal carcinoma in situ, 2 were Stage I1
cancers, and the remaining 18 were Stage I cancers,
Four nonwhite women were diagnosed with cancer,
CANCER October I , 1996 I Volume 78 I Number 7
Characteristicsof Women with Abnormal Screening Mammography, University of California San Francisco
Mobile MammographyProgram, July 1993-May 1994
Mean age (yr)
Family history of breast cancer
Report of palpable breast mass
First mammography screen (baseline)
Median income
(n = 203)
(n = 114)
Test statistic
32 (16%)
15 (7%)
87 (43%)
5 (4%)
9 (8%)
85 (75%)
x2 = 9.2
xz = 0.03
xz = 29.6
P value
NS: not statistically significant.
Outcomes of Women with Abnormal Screening Mammography,University of California San Francisco Mobile
Mammography Program, July 1993-May 1994
(n = 203)
(n = 114)
Test statistic
P value
Suspicious or malignant screening
mammography interpretation
Mean number of diagnostic tests
Median time from abnormal mammography
to final disposition (days)
Median time from abnormal mammography
to first diagnostic test (days)
Number of carcinomas
10 (5%)
3 (3%)
x2 = 0.97
t = 25G.5
Z = 2.98
4 (4%)
Z = 5.63
x? = 7.37
26 (13%)
NS: nnt statistically significant.
one Asian woman at Stage 11, one Latina at Stage I,
and two Latinas with ductal carcinoma in situ. Overall,
white women in our study group were more likely to
be diagnosed with cancer ( P < 0.01).
Diagnostic Tests
The vast majority of women (85%) underwent additional mammography views as the first follow-up test.
A total of 265 women (84%)underwent spot-compression magnification views, and 24 women (8%) began
their evaluation with ultrasound. Twenty-four women
(8%) began their diagnostic evaluation with an invasive procedure, 9 with fine-needle aspiration and 15
with biopsy (excisional or core biopsy). Of these 15
women who went directly to biopsy, 6 were diagnosed
with breast cancer.
Among the 13 women who had screening mammography interpreted as “suspicious” or “malignant,”
4 went directly to fine-needle aspiration or biopsy.
Eight were diagnosed with cancer. Three women completed their diagnostic evaluation within 1 week, five
within 1 month, and five within 2 months (range, 51
to 65 days). Three of these women were nonwhite;
their diagnostic evaluations were completed between
20 and 51 days after the date of index abnormal
screening mammography.
Evaluation of Mammographically Detected Abnormalities
It appeared that a wide range of evaluative tests were
performed on these women with abnormal mammography. To more closely examine this variation, we focused on women who had screening mammography
interpreted as “additional evaluation needed” and
had no palpable lesion. In other words, we looked
at the range of evaluations among 283 women who
presumably had abnormalities detected only by
screening mammography. Table 3 illustrates both the
range of final diagnostic tests conducted on these
women and the various routes used to reach a final
diagnosis or disposition. The majority of these women
(61%) underwent spot-compression magnification
mammography (magnification views) alone for resolution of their abnormality. Six women underwent fineneedle aspiration alone, and 10 women went directly
to biopsy. In all, 67 of these 283 women (24%) with
abnormal mammography interpreted as “additional
Race Difference in Mammography Follow-UplChang et al.
Description of Diagnostic Tests for Women with Mammographically
Detected Lesions Interpreted as “Additional Evaluation Needed”
Diagnostic tests
Repeat screening mammography
Spot-compression magnification mammography
With spot-compression magnification
Fineneedle aspiration
With spot-compression magnification
mammography and/or ultrasonography
With spot-compression magnification
With spot-compression magnification
mammography and ultrasonography
With fine-needle aspiration with or without
(n = 180)
(n = 103)
1 (0.6%)
1 (1.0%)
104 (57.8%)
18 (10,0%)
69 (67.0%)
14 (13.6%)
4 (3.9%)
5 (2.9%)
52 (28.9%)
15 (14.6%)
P value
F value
The same statistical results were found when substituting two other income variables, percentage of zip
code area households with incomes below poverty
level and income dichotomized at $20,000. Analysis
specifymg nonwhite racial/ethnic groups found that
each group (African American, Latina, and Asian) had
significantly longer log time to first diagnostic test
compared with white women ( P < 0.01 for each group)
but not compared with one another ( P > 0.05). The
same statistical results were found when performing
multivariate analysis of predictors of time to final diagnosis/disposition (log transformed).
Because prevalence of first screening mammography differed by race, we tested a model (not shown)
that included whether the index mammography was
a baseline examination; this did not alter the multivariate model results. Similarly, the age variable was categorized to compare women younger than 65 to those
age 65 and older (based on previous reports of later
cancer diagnostic stage for older womenlo).Using this
cut point and a continuous variable, patient age was
not a significant predictor of log time to first test in
the multivariate model.
Multivariate Analysis of Predictors of Time from Abnormal
Mammographyto First Diagnostic Testa (n = 315Ib
Independent variable
Age 50 yr or older
Palpable mass
Family history of breast cancer
Suspicious or malignant interpretation
ot screening mammography
Median income
Log transformation of time (to meet assumptions of normality:.
Nor inclriding two women for whom there was missing incomc! data (no zip code match).
Mod&adiusted R-square = 0.087, F value = 4.88.
evaluation needed” and no reported palpable mass
underwent biopsy. White women were more likely to
undergo biopsy than nonwhite women ( P < 0.02).
Among this group of 283 women, 22 (8%)were diagnosed with cancer; all but 1 were white.
Multivariate Model
Time to first diagnostic test (log transformed) differed
significantly for white compared with nonwhite
women ( P < 0.001) controlling for patient age, presence of a palpable breast mass, family history of breast
cancer, screening mammography interpretation, and
median income of residence zip code area (Table 4).
Definitions of timeliness of follow-up have varied, with
published reports measuring either time from index
abnormal screening mammography to first subsequent evaluative test or to final test/disposition. This
report focuses on absolute time of follow-up as opposed to rates of follow-up based on a defined cut
point for timeliness (i.e., within 8 weeks) because the
absolute timing is more specific and clinically relevant.
We found that there may be significant differences
between white and nonwhite women in the process
of evaluating abnormal screening mammography. Although rates of mammography screening have improved among women of ail raciallethnic group^,'^
there may still be barriers to timely performance of
subsequent evaluation of abnormal mammography
that differ by raceIethnicity.
Although there is little published literature on the
timing of follow-up in the evaluation of abnormal
mammography, a recent review of unpublished data
has shown some significant bivariate predictors of
longer follow-up times, including age (women older
than 65) and lower socioeconomic tatu us.'^ Our data,
using multivariate analysis, did not find age to be a
significant independent predictor of timeliness of follow-up.
Data from the Henry Ford Health System found
racial differences in timely follow-up that could be
accounted for by adjusting for income, with women
of lower socioeconomic status (median income less
CANCER October 1,1996 / Volume 78 / Number 7
than $20,000) being less likely to have timely followup compared with women with higher incomes.2"Our
results-using a continuous outcome variable (log
time to first diagnostic test)-detected such a racial/
ethnic difference when controlling for income, most
likely due to greater statistical power. Using less powerful logistic regression techniques to examine followup within 30 days (a dichotomized outcome), we
found that race lost its statistical significance in multivariate analysis.
The time involved in completing follow-up tests
will be affected by a variety of conditions but may
reflect delays related to the health-care system, patient, or p r ~ v i d e r . ~First,
~ , ~patient
~ , ~ ~-induced delay
may be related to individual fears or anxieties. A study
of women who have had abnormal screening mammography found significant amounts of anxiety associated with the test, with higher rates among those
with more suspicious reading^.^' RaciaUethnic differences in rates of fear and anxiety have also been reported in the context of routine mammography
~ c r e e n i n g . ~Similar
' ~ ~ ~ effects in the context of abnormal mammography screening may contribute to delay
in seeking or scheduling additional diagnostic tests.
Once women experience breast symptoms, there
have been reports of significant racial/ethnic differences in the timing of seeking care. Vernon et al.32
found that Latina and African American women had
significantly longer delays from the time of noticing
symptoms to time of first physician consultation. A
more recent study examining patient delay in seeking
breast care after onset of symptoms focused on white
versus African American women and failed to reveal
any significant d i f f e r e n ~ e . ~ ~
Second, provider-related delay may contribute to
our findings. Timely communication may be more difficult for nonwhite women if they predominantly receive their care through overburdened community
and public health clinics. Although women were required to provide the name and address of a primarycare provider before undergoing screening mammography, these names and addresses were not validated
at that time. The UCSF Mobile Mammography Program, however, has a tried-and-tested computer system to provide written notification of abnormal test
results to both referring providers and women who
have undergone screening. Referring providers also receive telephone notification of all screening-detected
abnormalities on the day after examination.
The effectiveness of communication between providers and patients may also differ, especially for those
patients whose primary language is not English but
who are likely to have English-speaking providers. It
is noteworthy that all women and their primary physi-
cians in our study received identical information (in
English only), emphasizing the need for prompt follow-up after abnormal mammography screening. It is
also important to note that we found no significant
racial/ethnic differences in the time from first to last
diagnostic test. This suggests that follow-up care proceeded in a timely manner for all women once diagnostic testing was begun.
Third, nonwhite women may have poorer access
to care (e.g., more likely to have public or no insurance, no regular care site or provider, and/or difficulty
maneuvering within a health-care system). All the
women included in our study had access to screening
services, but we had no information on their access
to subsequent diagnostic services or the continuity of
their care. Access difficulties may similarly be reflected
by the fact that nonwhite women were more likely
to be undergoing a baseline (or first-time) screening
mammography than the white women in our sample.
We have also described a wide range of practice variation in the evaluation of abnormal screening mammography cases. Whereas women were screened as
part of a single program, subsequent diagnostic evaluation occurred in many facilities throughout the San
Francisco Bay Area. This variation therefore reflects
clinical practice in both private and public systems of
health-care delivery. The racial difference described,
with white women being more likely to undergo biopsy, may be more appropriate given their higher observed cancer incidence rate in our series. The differing patterns of follow-up care by race maj. also be
related to women's socioeconomic status or to differences in practice style by site or provider. A lower rate
of invasive testing (i.e., biopsy) among nonwhites in
our series is consistent with reports of racial differences in the evaluation of other disorders, namely cardiovascular disease34and cerebrovascular disease.35
These studies have primarily focused on white versus
African American populations and have raised questions concerning potential differences in patient preferences, insurance coverage, and discriminatory practices among providers.
This report is based on a limited series of patients
accrued over a 10-month period. Although follow-up
information was collected on almost every woman
with abnormal mammography during the study period, many reports of follow-up testing were supplied
by primary-care providers. With the emphasis on the
patient's final diagnosis or disposition, they niay have
underreported the total number of diagnostic tests.
'Therefore, our report may underestimate the relative
differences in the timeliness of follow-up based on
race/ ethnicity. The statistical findings of our multivariate results, however, did not change when we excluded
Race Difference in Mammography Follow-UplChang et al.
from the analysis those women for whom we estimated (rather than ascertained) the dates of final diagnosis or disposition.
The database does not provide reliable, individual-level insurance information, so income (estimated
by zip code area) was used as a proxy measure for
slocioeconomic status. Although similar methodologies have been used in population-based studies,’”the
range of incomes within the San Francisco Bay Area
may not be reflected adequately by using median income values. Other studies have used percentage of
the population within the zip code area with incomes
below poverty level as a predictor of health service
We used this variable as well, with no
change in the results of our multivariate analysis.
The San Francisco Bay Area is not reflective of the
IJnited States population as a whole because of its
raciallethnic diversity and its generally higher rates of
mammography screening. Programs for both mammography screening and subsequent diagnostic testing, when necessary, are also available to women with
low incomes and with no health insurance. The setting
of our report, therefore, may reflect a “better case scenario” in terms of service availability and timeliness
of follow-up.
The clinical implications of longer follow-up times
after abnormal mammography screening are not
known. Screening mammography detects a higher
proportion of early stage breast
and the
median doubling time for mammographically detected tumors is long (median, 260 days).36 Consequently, it is likely that the relatively small, albeit significantly longer, time to completion of diagnostic
workup for nonwhite versus white women in our study
(median times, 19 days versus 12 days, respectively)
has had no impact on breast cancer stage or mortality.
It must be emphasized, however, that this difference
in workup time occurred in the setting of a well-organized system of follow-up and reporting of results. The
finding of raciaUethnic differences in our setting is
worrisome. It is possible that larger, potentially more
important raciallethnic differences may be observed
in clinical settings where reporting and follow-up procedures are not so complete.
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