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Causes of Physician Delay in the Diagnosis of Breast Cancer
William H. Goodson III, MD;
Dan H. Moore II, PhD
Arch Intern Med. 2002;162:1343-1348.
ABSTRACT
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Background Understanding sources of physician delay in diagnosis of breast cancer
will assist efforts to expedite diagnosis.
Objective To test whether increased reliance on screening mammography has affected
causes of physician delay in diagnosis of breast cancer.
Design Survey of delays in a case series.
Setting Practice specializing in breast diseases in a region with high use of
screening mammography.
Patients Four hundred thirty-five consecutive patients treated for 454 breast
cancers of any stage.
Intervention Customary patient care.
Main Outcome Measures Whether delay was related to how cancer was identified, patient age,
individual cancer characteristics (such as tumor type), mammography reports,
or physician expertise.
Results Twenty-one women (5%) were inappropriately reassured that a malignant
lump was benign without biopsy, 14 women (3%) had a misread mammogram, 4 women
(1%) had a misread pathologic finding, and 5 women (1%) had cancer missed
by a poorly performed fine-needle aspiration biopsy. Delay was associated
with a benign mammography report (relative risk, 10.8; 95% confidence interval,
5.1-22.8), a woman finding her own mass (relative risk, 3.3; 95% confidence
interval, 1.8-6.2), and current hormone replacement therapy (relative risk,
3.1; 95% confidence interval, 1.2-8.5).
Conclusions The leading cause of physician delay in diagnosis of breast cancer continues
to be inappropriate reassurance that a mass is benign without biopsy. Reducing
delay in diagnosis will require less willingness to rely on clinical examination
to decide that a mass is benign, less reliance on benign mammography reports
to decide not to biopsy a mass, and a requirement that fine-needle aspiration
biopsy be done by persons with demonstrated competence for the procedure.
INTRODUCTION
PHYSICIAN DELAY in the diagnosis of breast cancer is common. In previous
studies,1-6
6% to 16% of women with breast cancer experienced physician-caused delay in
diagnosis. This suggests that at least 10 000 of 180 000 women diagnosed
as having breast cancer each year experience delay of treatment because of
misinterpretation or misapplication of tests by their physicians. (This is
in contradistinction to delay when patients avoid seeking care for themselves.2, 7-10)
Historically, the leading cause of physician delay has been inappropriate
reassurance that a palpable mass is benign, without biopsy, with or without
reliance on mammography.2-3,5-6
Delay has been associated with younger patients2, 5, 8, 11-12
and chief complaints other than a mass.7-8
Most cancers in these prior studies were discovered as palpable masses. However,
because more breast cancers are now found by screening mammography, the causes
of delayed diagnosis may have changed. The possibility that mammography may
lead to different causes of delay is important, because surveys of patients'
experiences suggest that some physicians are replacing clinical breast examination
(CBE) with mammography.13-14
To study whether increased use of mammography has affected causes of
physician delay, we evaluated causes of physician-delayed diagnosis of breast
cancer in a contemporary series of patients in California, where 75% of women
aged 40 years and older have routine mammography at least every 2 years.15 We compared our results with similar surveys in an
attempt to understand whether delays result from failure by individuals or
limitations of widespread medical practices. Our purpose was to propose ways
to reduce delay.
PATIENTS AND METHODS
From January 1, 1992, through December 31, 1999, we prepared short clinical
abstracts from the medical records of 435 consecutive patients with 454 breast
cancers of any stage referred from multiple sources to one surgeon (W.H.G.).
For this analysis, bilateral cancer was counted as 2 cancers. Multiple foci
of cancer in 1 breast was counted as 1 cancer. Information from these abstracts
was put into a database (FileMaker Pro; Claris Corporation, Santa Clara, Calif)
for analysis with standard statistical programs (Excel; Microsoft Corporation,
Redmond, Wash; Data Desk; Data Description Inc, Ithaca, NY; and Stata, Stata
Corp, College Station, Tex).
A detailed history was obtained from each patient at the initial visit. Chief complaint was defined as the first observation (by
the patient, her physician, a radiologist, or other) that made the patient
aware of the abnormality that was eventually diagnosed as cancer, without
regard to how or by whom diagnostic tissue was obtained. We use diagnosis strictly to denote confirmation of cancer by histological
or cytological examination. The history of whether the patient had been reassured
that a mass was benign without biopsy was based on the patient's understanding
of what she had been told. Other information was corroborated by review of
medical records, mammograms, histological slides, and other sources. We defined delay as physician action that completed an episode of
care without diagnosing cancer of which there was a sign. Delay was tabulated
if (1) a physician acknowledged a breast abnormality on physical examination
but reassured the patient, without biopsy, that the mass was benign, and biopsy
of that abnormality found cancer (offering a biopsy was not considered a mitigating
action if biopsy had not been encouraged); (2) a fine-needle aspiration biopsy
(FNA) obtained no malignant cells from a palpable or mammographic lesion,
and cancer was found with a subsequent FNA by a physician with formal training
in the procedure; (3) palpation-guided FNA obtained no malignant cells from
a mammographic lesion, the patient was reassured, and subsequent image-guided
biopsy found cancer; (4) a written pathology report indicated benign tissue
and another pathologist diagnosed cancer on the same slides; or (5) a mammography
report did not recommend biopsy or short-interval follow-up, review of the
original x-ray films found suspicious calcifications or change, and biopsy
confirmed cancer at that site. Length of delay was counted from physician
action until diagnostic steps were resumed.
Physician delay was not tabulated if the responsible physician recommended
a mammogram or a second physical examination after a short interval, if the
physician recommended another diagnostic procedure, or if the original mammograms
were unavailable.
As factors associated with delay in diagnosis, we examined chief complaint
at the time of diagnosis, age, menopausal status, current hormone replacement
therapy (HRT) in women after menopause, tumor type and grade, and interpretation
of mammogram and FNA (if performed).
RESULTS
Four hundred thirty-five women and 1 man underwent surgery for 454 cancers
during the study (median age, 54 years; range, 24-88 years). Nineteen women
had a second cancer in the contralateral breast. Data are analyzed as 454
separate cancers occurring in 454 separate breasts. No patient had delay in
the diagnosis of both breasts. As shown in Table 1, the most common chief complaint for women younger than
50 years was the patient finding a mass, whereas for women 50 years and older,
the most common chief complaint was a suspicious mammographic finding.
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Table 1. Chief Complaints That Initially Made Patients Aware of Breast
Abnormalities at the Time of Diagnosis*
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Delay occurred for 42 (9%) of 454 cancers. Nineteen (11%) of 175 cancers
diagnosed before referral had delay, compared with 23 (8%) of 279 cancers
diagnosed after referral ( 2 = 0.87; P
= .22). Nineteen (45%) of 42 cancers with delay had diagnosis before referral,
compared with 156 (38%) of 412 cancers without delay. The median delay was
9 months (range, 1-36 months), with a delay of 3 or more months for 30 patients
and 6 or more months for 24 patients.
Twenty-one women (5%) were inappropriately reassured by their physician
(15 primary care physicians and 6 consultant surgeons) that a lump was benign
without biopsy. Fourteen (3%) had mammogram interpretation that failed to
note a new mass (8 patients) or suspicious calcifications (6 patients). One
mammography report noted a benign cyst but overlooked 5 cm of microcalcifications.
(The 2 patients with misread mammograms and inappropriate reassurance are
counted in both categories; Table 2).
Four patients had misread pathology reports from a surgical biopsy. Three
had "benign" pathology reports, but review of the original histological slides
revealed ductal carcinoma in situ. One of these women died of invasive cancer,
identified by subsequent biopsy of residual calcifications in the same cluster.
One had a diagnosis of lobular carcinoma in situ, but review of the original
slides found ductal carcinoma in situ that required reexcision to obtain negative
margins. Five women had poorly performed FNA by a physician without formal
training in FNA technique, 3 by surgeons and 2 by other physicians. Four had
no malignant cells obtained by FNA of a palpable mass that was subsequently
diagnosed by FNA performed by a physician with specific training in FNA. Three
of these women had delays of 4 to 6 months; 1 had workup resumed within a
month when her overdue, routine mammogram showed suspicious microcalcifications.
One patient with suspicious mammographic findings had benign results on a
palpation-guided FNA of an area her surgeon assumed was the same as the area
of suspicion on the mammogram, but subsequent image-guided biopsy found cancer,
ie, her physician did an FNA in the wrong area.
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Table 2. Chief Complaints at the Time of Diagnosis After Various Types
of Initial Delays
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None of the women with misread mammograms, misread pathologic findings,
or poorly performed FNA were aware of delay before referral. Seventeen of
21 women with inappropriate reassurance were diagnosed when they sought further
medical care (9 were diagnosed before referral; Table 2).
UNIVARIATE ANALYSIS
When women found their own lump, physician delay was 3 times more likely
than when cancer was found by mammography, physician examination, or another
sign (relative risk, 3.3; 95% confidence interval, 1.8-6.2; Table 3).
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Table 3. Univariate Analysis of Factors Possibly Relating to Delay*
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Physician delay was 10 times more likely for women with a benign mammography
report (relative risk, 10.8; 95% confidence interval, 5.1-22.8; P<.001). Fourteen so-called benign mammograms were incorrectly read,
but 21 were correctly read (for 17 women who received inappropriate reassurance
and 4 who had poorly performed FNA biopsy). Among women who found their own
lump, 22 (32%) of 69 cancers with benign mammographic findings had delayed
diagnosis, but only 3 (4%) of 78 cancers with a suspicious mammographic finding
had delayed diagnosis (relative risk, 7.9; 95% confidence interval, 2.4-25.3).
One hundred sixty cancers were in premenopausal women, 15 were in perimenopausal,
and 271 were in postmenopausal women (data unavailable for 7). Among the cancers
in postmenopausal women, more delays occurred among the 122 cancers in women
taking HRT at the time of diagnosis than among the 137 cancers in women not
taking HRT (relative risk, 3.1; 95% confidence interval, 1.2-8.5; P = .02; Table 3). Also
among the postmenopausal group, all 8 instances of inappropriate reassurance
occurred in women taking HRT (2 = 9.3, P = .002). For women in the postmenopausal group who found their own
lump, 8 of 26 taking HRT received inappropriate reassurance, compared with
none of 34 not taking HRT (2 = 12.1; P<.001).
Delay was less likely for ductal carcinoma in situ than for invasive
cancers. However, 66 (71%) of 93 ductal carcinoma in situ were identified
by mammography vs 129 (40%) of 325 invasive cancers, so this difference may
reflect expedited follow-up of abnormal mammographic findings rather than
a factor predisposing to less delay.
There was a trend for more delays with low-grade tumors (P = .06). Delay was not associated with lobular vs ductal histological
findings or age, nor was age associated with a specific cause of delay.
Physician delay was not associated with outcomes of larger tumor size,
more positive nodes, or higher likelihood of having a mastectomy (Table 4). However, 4 of 24 women with more
than 6 months' delay filed malpractice claims against the responsible physician.
These women were ages 40, 44, 47, and 55 at the time of diagnosis.
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Table 4. Outcomes That Might Be Influenced by Delay in the Diagnosis
of Breast Cancer
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MULTIVARIATE AND HIERARCHICAL ANALYSIS
In multivariate logistic analysis, a woman finding her own mass and
taking HRT were statistically significant variables (P
= .004 and P = .049, respectively). In a hierarchical
model, benign mammographic findings and a woman finding her own mass were
significant factors within the group of women taking HRT (P<.001 and P = .03, respectively). Among
women who found their own mass, a benign mammographic finding was a significant
factor (P<.001), and current use of HRT was marginally
significant (P = .06).
COMMENT
Despite widespread screening mammography, inappropriate reassurance
that a palpable mass is benign, without biopsy, remains the leading cause
of physician-delayed diagnosis of breast cancer, affecting 5% of patients
in our series. Combining all causes, 9% of patients experienced delay.
Thirty-five percent (161/454) of cancers were first identified by patients
themselves, but a disproportionate 64% (27/42) of the delays occurred when
the patient first identified their own mass. This is consistent with analyses
of physician delay2, 5-6
and malpractice lawsuits,16 which found that
physician reassurance that a self-discovered mass was benign was a major cause
of delay.
The known higher false-positive rates for breast self-examination may
explain the association between delay and self-discovery. In randomized trials
of breast self-examination, women who did breast self-examination found, in
addition to cancer, many extra benign masses that required evaluation.17-18 Physicians seem to intuit lower cancer
risk for self-discovered masses and seek to reassure patients using CBE or
mammography, without performing biopsy.
There are 2 possible responses when a patient identifies a breast mass.
One approach is to interpret what the patient has felt and to reassure the
patient without biopsy if the physician believes that the mass is benign.
We do not know how often such reassurance is given in practice, but 21 of
our patients experienced delayed diagnosis because of such misinterpretation
of a mass by their physician. Seventeen of these women had mammograms with
no signs of cancer even in retrospect, ie, they had false-negative mammograms.
The potential for a negative mammogram to contribute to misinterpretation
of CBE is an old finding.1, 3-4,6, 16
Because of a trend to substitute mammography for CBE,13-14
inappropriate reliance on mammography may become a greater problem.
The alternative is to encourage diagnostic tissue sampling from all
palpable breast masses.1 Fine-needle aspiration
is the least invasive way to obtain tissue, but 1% of our women experienced
delay because FNA was attempted by an untrained physician. Similarly, Ljung
et al19 found that tissue sampling by physicians
without formal training in FNA technique missed 25% of cancers, while physicians
with formal training missed only 2% of cancers. The National Cancer Institute20 Consensus Panel recommended that FNA be done only
by persons with special training. Often this person is not a surgeon, but
examination by a surgeon is desirable before needle biopsy, which might cause
a hematoma. If no FNA-trained physician is available, surgical or core biopsies
are alternatives.
Clinical breast examination is an inexact science, and there may be
legitimate questions of whether a mass exists. Such judgments are difficult.
Haagensen,21 in the era before widespread mammography,
described the "humiliating experience" of being shown a mass by a patient
after his own detailed examination. A second examination after a short interval
allows a fresh perspective to decide whether a mass exists and would have
provided a second chance for prompt diagnosis for the 21 women who were inappropriately
reassured. This is an accepted plan,21-23
especially for women before menopause, whose breasts change cyclically.
Breasts also have varying areas of nodularity and density, and there
may be limited, defined situations in which it is appropriate to reassure
patients without biopsy. Such changes must be symmetrical in both breasts
or be anticipated in the context of life events, such as prior biopsy.23 For example, breast tissue is typically more dense
in the upper outer quadrant. If both breasts are symmetrically more dense
in this area, this is likely the patient's normal condition. Similarly, nodularity
may increase after weight loss or when hormone effects subside, eg, after
pregnancy.23 These changes are not focal, as
are most cancers, and they do not explain a single, self-discovered mass.
Like Tartter et al,6 who also studied
various chief complaints, we did not find a relation of age to delay. However,
malpractice litigation was filed only by 4 younger women, which agrees with
the observation that malpractice plaintiffs are younger than the average woman
with breast cancer.16 Prior reports2, 5, 8, 11 linking
delay to younger age included mainly women with self-discovered or palpable
masses, rather than a spectrum of chief complaints, which likely explains
the difference.
Like Richards et al,10 we found a trend
for less delay among women with high-grade tumors. As Coates24
suggested, this may be because high-grade tumors are clinically more obvious,
perhaps demonstrating greater tissue reaction to the cancer, and receive expedited
care.
More frequent delay with HRT, particularly inappropriate reassurance,
is a new observation. Hormone replacement therapy decreases sensitivity of
mammography, probably because increased tissue density hides early signs of
cancer.25 However, sensitivity of CBE is not
the issue when inappropriate reassurance is given for a mass that has already
been discovered. We suspect that knowledge of the effects of HRT on mammographic
density26 is somehow extrapolated into a supposed
explanation of why a mass is present in a given patient.
All diagnostic tests for breast cancer have known rates of misinterpretation.
In our series, 217 cancers were first identified by mammography, but 14 (7%)
had delay because of misinterpretation of mammograms. In other studies,3, 27-28 reading of mammograms
by a single radiologist missed 5% to 10% of cancers. Similarly, pathologists
misread 1% of our cases, and others report misinterpretation of pathologic
findings for 0.7% to 4% of breast cases.29-31
Review by a second radiologist or pathologist reduces misinterpretation of
these tests.3, 27, 30
Misinterpretation is also a known characteristic of CBE, as observed
in previous surveys.1, 3, 6-7
In our series, 21 women had misinterpretation of CBE, 6 times by consultant
surgeons. In a direct assessment of ability to classify masses, Hicks et al32 found that 18 of 197 masses classified as benign
on CBE were malignant.
Unlike mammography and pathologic examination, however, second interpretation
of a CBE does not greatly improve accuracy. When Chamberlain et al33 tried to increase accuracy, they found that, when
2 physicians examined 215 women with a family history of breast cancer, 4
of 6 cancers were in women whom both physicians agreed not to refer for biopsy.
Similarly, the Yorkshire Breast Cancer Group34
found only 59% agreement between clinicians on whether to categorize masses
as malignant or benign.
For precisely the reason that interpretation of CBE is an inexact science,
once a mass is identified, there must be the equivalent of a second reading,
but neither mammography nor another CBE is sufficient. Only tissue sampling
is adequate. If a mass is followed up without biopsy, patients should be informed
that interpretation of CBE has a known rate of misinterpretation even with
an experienced examiner. Unless tissue sampling is encouraged, we view simply
mentioning a biopsy as nothing more than self-protecting behavior by the physician.
Because this was a single practice, we cannot comment on the true frequency
of delay in our community. However, because the proportion with delay was
similar among women diagnosed before and after referral, and because the proportion
of patients referred after diagnosis was similar in the delay and the nondelay
groups, we know of no reason to suspect biased referral of a particular type
of delay, and identification of factors associated with delay should not be
affected. Furthermore, our data set has allowed us to investigate novel factors
in delay, such as different chief complaints, the role of FNA, and current
use of HRT.
These delays began when 42 different physicians used tests—interpretation
of CBE, single interpretation of mammograms and pathologic findings, and FNA
by untrained (but otherwise experienced) persons—that have known rates
of inaccuracy. The performance characteristics of these tests (discussed herein)
predict delay will occur at random in practices whenever these tests are widespread
in the medical community. Therefore, we believe that most delayed diagnoses
reflect not failures by individuals but, rather, the overall inadequacy of
practices that are accepted, despite the fact that they fail even in experienced
hands. Reeducating a few physicians will not eliminate delayed diagnosis.
Rather, reducing delay will require collective changes in all clinicians'
perception of whether to interpret CBE, the reliability of mammography, whether
to demand that tests like FNA be performed well or simply performed, and possibly
how to interpret the secondary effects of HRT. To reduce physician delay,
we suggest that physicians provide care with "FERVR":
- Focus CBE on the presence
or absence of a mass, without interpretation of what it might be.
- Expect tissue sampling
for all palpable breast masses.
- Recommend tissue sampling
of all palpable masses even if the mammogram shows no signs of cancer.
- Verify that physicians
doing FNAs on their patients have specific training in the procedure.
- Reevaluate patients after
a short interval if a tentative decision is made that an area identified by
a patient falls within the narrowly defined rules of predictable variations
of breast structure.
AUTHOR INFORMATION
Accepted for publication October 22, 2001.
This study was presented in part at the Second European Breast Cancer
Conference, Brussels, Belgium, September 29, 2000.
We thank Brian Mayall, MD, and Stefanie Jeffrey, MD, for constructive
criticism during the preparation of the manuscript.
Corresponding author and reprints: William H. Goodson III, MD, Department
of Surgery, California Pacific Medical Research Institute, 2100 Webster, Suite
401, San Francisco, CA 94115 (e-mail: whg3{at}cooper.cpmc.org).
From the Department of Surgery (Dr Goodson) and the Geraldine Brush
Cancer Research Institute (Dr Moore), California Pacific Medical Research
Institute, and the Department of Epidemiology and Biostatistics, University
of California, San Francisco (Dr Moore).
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