Factors Associated With Adequacy of Diagnostic Workup After Abnormal Breast Cancer Screening Results
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J Am Board Fam Pract: first published as 10.3122/15572625-13-2-94 on 1 March 2000. Downloaded from http://www.jabfm.org/ on 21 February 2022 by guest. Protected by copyright.
ORIGINAL ARTICLES
Factors Associated With Adequacy of Diagnostic
Workup After Abnormal Breast Cancer Screening
Results
Mario Schootman, PhD, Jill Myers-Geadelmann, RN, and Laurence Fuortes, MD
Background: Women with certain characteristics, such as those residing in rural areas, are less likely
screened for breast cancer. To enhance detection of early breast cancer, it is imperative that all women
who have abnormal screening results receive appropriate diagnostic procedures. This study reports
differences in receipt of diagnostic services following abnormal screening results.
Methods: Screening and diagnostic data were collected as part of a breast and cervical cancer early
detection program aimed at reaching women of lower socioeconomic status. Women with completed
diagnostic information after having abnormal screening results were included. We based adequacy of
diagnostic services on guidelines from the Society for Surgical Oncology, The Commission on Cancer of
the American College of Surgeons, and the Centers for Disease Control and Prevention. Several factors
were assessed for their association with adequacy of diagnostic follow-up: income, age, race, education,
health insurance status, rural-urban residence, reported breast lump, family history of breast cancer,
and clinical beast examination or mammogram results.
Results: Overall, 14.1% of the 351 abnormal findings were considered inadequately followed up
based on the algorithm used. Eighty percent involved an abnormal finding on a clinical breast examina-
tion regardless of the mammogram results. Rural women, those with abnormal clinical breast examina-
tion findings but normal or equivocal findings on mammograms, and those who self-discovered a mass
were less likely to receive adequate follow-up than were their counterparts in multivariate analysis.
Rural women were less likely to receive a biopsy or fine-needle aspiration, although it was indicated.
One facility accounted for most of the inadequate follow-up screenings among urban women.
Conclusions: Women who have specific demographic and clinical characteristics were less likely to
have received adequate diagnostic services. Breast cancers could have been missed initially as a result
of inappropriate follow-up. Further investigation of the clinical scenarios using chart reviews is war-
ranted. (J Am Board Fam Pract 2000;13:94-100.)
Screening for breast cancer is considered beneficial status, being limited physically, belonging to a mi-
when conducted at recommended intervals. 1 Un- nority group, and residing in rural areas, were less
fortunately, not all women receive screening to an likely to be screened for breast cancer.2 Reasons for
equal extent. Women who have specific character- lower screening utilization include fewer primary
istics, such as occupying a lower socioeconomic care physicians in rural areas and access to those
physicians, in particular because the clinician's rec-
ommendation is the main reason women receive
Submitted, revised, 21 September 1999. mammograms. 3
From the Division of Health Behavior Research (MS), To enhance survival following detection of
Departments of Internal Medicine and Pediatrics, Washing-
ton University School of Medicine, and The Alvin J. Site- breast cancer, all women need to receive timely and
man Cancer Center at Barnes-Jewish Hospital (MS), St appropriate diagnostic services based on their
Louis, Mo; the Bureau of Health Promotion (MS, JM -G),
Iowa Department of Public Health. Des Moines; and the screening results. 4 Delay in establishing a diagnosis
Department of Epidemiology (LF), College of Public and initiating treatment can result in more ad-
Health, The University of Iowa, Iowa City, Iowa. Address
reprint requests to Mario Schootman, PhD, Division of vanced disease at the time of diagnosis and a worse
Health Behavior Research, Departments of Internal Medi- outcome. Delayed diagnosis also accounts for the
cine and Pediatrics, Washington University School of Med-
icine, 4444 Forest Park Parkway, Box 8504, St. Louis, MO most expensive and most common medicolegal
63108. claims against physicians. 5,6 The receipt of timely
94 JABFP March-April2000 Vol. 13 No.2J Am Board Fam Pract: first published as 10.3122/15572625-13-2-94 on 1 March 2000. Downloaded from http://www.jabfm.org/ on 21 February 2022 by guest. Protected by copyright.
services after abnormal screening results is influ- Methods
enced by such factors as screening results, clinic Iowa Breast and Cervical Cancer Early Detection
access, the number of diagnostic events per visit, Program
and access to specialty care 7 as well as patient char- The Iowa Breast and Cervical Cancer Early Detec-
acteristics. 8 tion Program (BCCEDP) was established to screen
Appropriate diagnostic services are essential eligible women for breast and cervical cancer. Eli-
components of a timely follow-up. Specific diag- gibility is based on household income, with women
nostic tests must be completed for the evaluation at or below 250% of the federal poverty guideline
and management of such breast problems as a pal- eligible to receive services at no cost. Emphasis is
pable mass or a nonpalpable mammographic ab- placed on screening women aged 50 years and
normality.9 For example, Osuch et al 5 suggest using older, although a percentage of women screened
a triple diagnosis in the management of a solid are younger than 50 years.
breast mass. This dramatically increases diagnostic Clinical services were delivered at the local level
accuracy. If a mass is interpreted as benign by all by more than 300 clinics, mammography facilities,
three methods (follow-up clinical breast examina- hospitals, and cytology laboratories. Women re-
tion, mammogram, and fine-needle aspiration), di- ceived usual care from the clinicians. Every woman
agnostic accuracy approaches 99%.10,11 had a primary care physician who was responsible
Additionally, the use of subsequent diagnostic for her care. No attempt was made to influence
procedures is imperative if there are abnormal find- delivery of screening and diagnostic work-up.
ings on a clinical breast examination a~d a normal
Data were collected by the Iowa BCCEDP as
mammogram. A number of breast cancers might be
part of a clinical service delivery monitoring effort.
missed because it is not possible to capture the
The Iowa BCCEDP consists of 26 local programs
posterior portion of the breast on the film, because a
spanning 49 counties, one half of all Iowa counties.
cancer cannot be visualized against a background of
Each local program is responsible for collecting
dense tissue, or because the radiologist misinterprets
data about women for which it is administratively
the film.n,12 Normal mammography findings in the
responsible.
presence of a palpable mass add no information.
Two forms were used for data collection, an
A common dilemma facing clinicians is how to
Intake and Visit Summary form and a Diagnostic
approach a patient-discovered mass that is con-
Results form. The intake form is completed for
firmed by physical examination but not visualized
each woman regardless of the type of screening
on a mammogram. s In the Physician's Insurance
service performed. Information contained on this
Association of America 1995 study, 60% of women
form includes demographics (name, birth date, ad-
who brought successful claims for failure to diag-
dress, race, ethnicity, highest educational level,
nose breast cancer had self-discovered masses that
household income), history (most recent screen-
failed to impress their physicians on clinical exam-
ination; 80% had normal or equivocal mammo- ing), self-reported breast symptoms, and breast and
cervical screening information (type, date and re-
gram resultsY
As with screening utilization, women who share sult of clinical service). Initial mammographic find-
specific demographic characteristics might be less ings were reported using the Breast Imaging Re-
likely to receive follow-up diagnostic services. porting and Data System (BI_RADSTM).14 Clinical
Hence, our study will attempt to determine which breast examination findings were reported as nor-
women with questionable breast-screening results mal (not suspicious for cancer) or abnormal (suspi-
are less likely to receive diagnostic services. Specif- cious for cancer).
ically we will compare diagnostic services received Diagnostic information is completed when an
by rural and urban women. We will also examine abnormality is detected at screening. The Diagnos-
diagnostic service utilization by those who come to tic Results form contains the woman's identifying
the clinician's office having found a breast lump information and the types, dates, and results of the
and by those for whom findings on the clinical diagnostic services performed. A final diagnosis and
breast examination were abnormal and the mam- the diagnostic disposition are also included on the
mogram findings were normal. form.
Abnormal Breast Cancer Screening Results 95J Am Board Fam Pract: first published as 10.3122/15572625-13-2-94 on 1 March 2000. Downloaded from http://www.jabfm.org/ on 21 February 2022 by guest. Protected by copyright.
Table 1. Result of Clinical Breast Examination and Mammogram (n - 351) and Adequacy of Follow-Up.
Number
Algorithm (Rural, Urban) CBE Result Mammogram Result Diagnostic Procedures Required
122 Abnonnal, suspect cancer Negative At leost one
(57,65) Benign Repeat breast examination
Probably benign Surgical consultation
Assessment incomplete Sonogram
Biopsy or lumpectomy
Fine-needle or cyst aspiration
2 36 Abnonnal, suspect cancer Suspect abnonnality At /eost one
(26,10) Highly suggestive of Biopsy or lumpectomy
malignancy Fine-needle or cyst aspiration
3 83 Nonnal (do not suspect Suspect abnonnality At leost one
(65, 18) cancer)
Repeat breast examination
Surgical consultation
Sonogram
Biopsy or lumpectomy
Fine-needle or cyst aspiration
4 12 Any result Highly suggestive of At /eost one
(5,7) malignancy Biopsy or lumpectomy
Fine-needle or cyst aspiration
5 98 Nonnal (do not suspect Assessment incomplete At /eost one
(54,44) cancer) Additional mammographic views
Sonogram
CBE-clinical breast examination.
Data included in the analysis are those for which prepared by the Society for Surgical Oncology,
a final diagnosis is available during the period from The Commission on Cancer of the American Col-
August 1995 through September 1998. Only lege of Surgeons, and the Centers for Disease Con-
women with completed foHow-up were included in trol and Prevention.9 This descripton is a modifi-
the analysis, and those lost to follow-up or who had cation of a previously developed algorithm. ls Table
refused diagnostic procedures were excluded. Al- 1 lists the diagnostic procedures considered to be
though not all diagnostic services were reimbursed adequate based on the results of the clinical breast
by the Iowa BCCEDP, fine-needle aspiration, ad- examination and mammogram. Claims data, sub-
ditional mammographic views, and breast biopsies mitted independendy for provided services by the
were covered services. clinics, were used to corroborate the services re-
A total of 3198 clinical breast examinations and ported on the submitted Diagnostic Results form.
mammograms were performed during the study
period, and an abnormality was detected during
Statistical Analysis
351 of the breast examinations or mammograms.
Because of the prospective nature of the study, we
Diagnostic procedures were pending for 9 women,
modeled relations between variables and the de-
3 women were lost to follow-up, and 5 women
pendent variable (adequacy) using relative risks.
refused all diagnostic services. Thus, 95.6% of
women received diagnostic follow-up services. The proportional hazard approach was used to se-
lect factors associated with inadequately performed
follow-up services.
Definition 0/Adequacy Variables that were considered included income
For the current study, we defined adequacy of di- category «100% of poverty vs 101 % to 250% of
agnostic services according to Evaluation ofCommon federal poverty guidelines), age groups (younger
Breast Problems: A Primer for Primary Core Providers than 50 years vs 50 years and older), race (white vs
96 JABFP March-Apri12000 Vol. 13 No.2J Am Board Fam Pract: first published as 10.3122/15572625-13-2-94 on 1 March 2000. Downloaded from http://www.jabfm.org/ on 21 February 2022 by guest. Protected by copyright.
Table 2. Frequency of Inadequate Follow-Up and Associated Factors Using the Proportional Hazard Approach.
Likelihood Ratio Test
Demographic Characteristics Percent Relative Risk (P Value)
Age group 3.92 (.0478)J Am Board Fam Pract: first published as 10.3122/15572625-13-2-94 on 1 March 2000. Downloaded from http://www.jabfm.org/ on 21 February 2022 by guest. Protected by copyright.
50
• Rural tween rural and urban women. Among rural
40 women with abnormal findings on a clinical breast
., DUrban
~ 30 examination and mammograms, 48.0% did not re-
..
c
e 20 ceive a biopsy or lumpectomy or a fine-needle or
C>-
10 cyst aspiration while indicated by the algorithm. In
0
some cases, rural women with other clinical breast
2 3 4 5 examination and mammogram results did not re-
eBE/mammogram algorithm ceive appropriate diagnostic follow-up, such as for
Figure 1. Percentage of inadequately followed up algorithm 1 and 3.
abnormal breast cancer screening results, by clinical Among urban women all inadequate follow-up
breast examination and mammogram results. services were for those who had abnormal findings
on a clinical breast examination and normal find-
ings (or assessment incomplete) on a mammogram
1.03). Additionally, women who had screening re- (algorithm 1). In contrast, rural women had a vari-
sults listed in algorithm 1 were 0.47 times as likely ety of screenings for which they received inade-
to receive adequate follow-up services compared quate follow-up services.
with those with other clinical breast examination
and mammogram results (95% cr, 0.26 - 0.88).
The interaction between geographic location and Discussion
type of clinical breast examination or mammogram The aim of our study was to assess factors associ-
result could not be assessed because all urban ated with women of lower socioeconomic status
women with inadequate follow-up services had an receiving adequate diagnostic services after abnor-
abnormal clinical breast examination and normal mal results on breast cancer screening. Ninety-six
mammogram findings (Figure 1). percent of women with abnormal findings on breast
Although having felt a lump on breast self-ex- screening received diagnostic procedures, which
amination did not statistically predict adequacy of indicates that even women of lower socioeconomic
follow-up after inclusion of the clinical breast ex- status can receive these services when indicated.
amination or mammogram results and the resi- This percentage of women receiving diagnostic
dence of the woman screened, the regression coef- workup is much higher than that reported by a
ficients of the model containing both variables study using BCCEDP data in California 16 and is
changed to an important degree. Women who felt necessary to maximize screening benefits.
a lump were 0.57 times (95% cr, 0.30 - 1.06) as Rural women, those with abnormal clinical
likely to have received adequate follow-up services breast examination results and normal mammo-
than those who did not have any symptoms. gram results, and those who self-discovered a breast
The need to assure appropriate diagnostic ser- mass were less likely than their counterparts to
vices for a woman who self-discovers a mass, which receive an adequate diagnostic workup based on
is confirmed by the clinician, but who has subse- guidelines prepared by the Society for Surgical On-
quent normal findings on a mammogram is self- cology, The Commission on Cancer of the Amer-
evident. 9 Women with these results were 0.27 ican College of Surgeons, and the Centers for Dis-
times as likely to have adequate follow-up services ease Control and Prevention. 9 None of the other
as those who did not feel a mass on examination variables were associated with less-than-adequate
and had other clinical breast examination and follow-up services. Even women without health
mammogram results. insurance, minority women, and those living in
poverty received diagnostic services similar to those
Types of Inadequate Diagnostic Workup received by their counterparts. Because women
Of all screenings among women who did not re- with these characteristics are typically less likely to
ceive appropriate follow-up according to the algo- be screened for breast cancer, our study shows that
rithm used (n = 50), 80.0% involved an abnormal it is possible to assure adequate follow-up diagnos-
clinical breast examination finding regardless of the tic services for these women.
result of the mammogram (algorithm 1 or 2). Dif- Rural women were less likely to receive appro-
ferences in inadequate follow-up were found be- priate diagnostic services in our study. The main
98 JABFP March-Apri12000 Vol. 13 0.2J Am Board Fam Pract: first published as 10.3122/15572625-13-2-94 on 1 March 2000. Downloaded from http://www.jabfm.org/ on 21 February 2022 by guest. Protected by copyright.
reason for inadequate follow-up among rural sively studied in relation to the diagnostic workup
women is underuse of biopsy and fine-needle or of their abnormal breast screening results.
cyst aspiration among those with both abnormal One limitation of the study is the use of the
findings on clinical breast examinations and mam- algorithm. Although several agencies and organiza-
mograms (algorithm 2). A proportion of these tions were involved in the development of the
women might have had their condition initially guidelines, it is not possible to describe every clin-
misdiagnosed as not being breast cancer and later ical situation. It is expected, however, that the over-
have more advanced disease. all results did not suffer from this limitation. More-
In contrast with the distribution of the percent- over, from a system point of view, the results
age of rural women with inadequate follow-up provide valuable insight into where efforts need to
(Figure 1), all urban women with inadequate diag- be focused.
nostic services had abnormal clinical breast exami- A second limitation is that the results were based
nation findings and normal findings on a mammo- on relatively few cases. Rural-urban differences
gram (or assessment incomplete) as described in were close to being statistically significant, how-
algorithm 1. On closer examination, one clinic site ever, and we found a lack of appropriate workup
accounted for almost three out of every four among those with abnormal clinical breast exami-
screenings. nation findings and normal findings on mammo-
Based on the rural-urban differences and the grams. If more cases had been included, the results
percentage of inadequate follow-up services for would have been even more pronounced.
each of the five algorithms, it can be concluded that In conclusion, the results show important differ-
assurance of appropriate follow-up is warranted ences in screening results between rural and urban
populations. These analyses are only the first step
when there are abnormal findings on clinical breast
toward assuring that all women receive appropriate
examination and normal findings on a mammo-
diagnostic services. We have planned to investigate
gram. A significant percentage of breast cancers
further the clinical scenarios by using chart reviews.
will be missed when not performing adequate
workup of a breast mass. 9 Increasing emphasis has
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