Breast Cancer Missed by Mammography
Nondetection of breast cancer on mammography is of con- cern to the patient, the referring physician, and the radiolo- gist. Nondetection of cancer on mammography is the result of a variety of factors, including the mammographic technique, experience of the radiologist, morphology of the breast tumor, and the background on which it is displayed. Errors can occur at any levels, ie, in technique, in detection, and in interpre- tation (Table 2.9). Cancers can best be displayed by good mammographic technique, optimal positioning, and a tumor B
CC
Spot LMLO MLO
A
C
D
FIG. 2.35 Spot view workup for a possible mass. Final diagnosis: a summation artifact. (A and B) Mediolateral oblique (MLO; A) and craniocaudal (CC; B) screening mammograms; a possible mass is seen in the lower part of the left breast on the MLO view near the chest wall (circle with arrow) but not on the CC view. (C) A spot compression film shows no mass. (D) Ultrasound in this region shows fatty and scant fibroglandular tissue. This possible mass is overlapping tissue.
location that can be displayed on the film. Approximately 10%
to 15% of breast cancers are mammographically occult, even on good images, and will not be detected on mammography in the best of hands.
Missed cancers on mammography can be categorized into sev- eral types (Box 2.9). First, the tumor may have a morphology that is undetectable on the mammographic background on which it is displayed and is therefore mammographically occult. Second, the tumor may display findings that are visible, but below the thresh- old of any radiologist for consideration as cancer. Such findings have been termed nonspecific, examples of which include mam- mographic findings suggesting normal islands of fibroglandular tissue, a few benign-appearing calcifications, or a benign-appear- ing mass among many other benign-appearing masses that do not represent cancer. Third, the tumor may show subtle findings that represent cancer but are atypical, such as a single dilated duct, a developing asymmetry, or other less common features of breast cancer that are perceptible but may have been unrecognized.
Fourth, signs that are classic for breast cancer may have been present on the mammogram but either were not perceived or were misinterpreted at the time of diagnosis.
Box 2.10 shows mammographic features of missed cancer, according to the review of previous studies. Birdwell et al. (2001)
reviewed possible reasons why cancers were not identified on previous mammograms. They postulated that findings were hid- den among many other findings (“busy breasts”) or that distract- ing findings other than the cancer were present on the film.
Other contributing factors included dense breast tissue, small calcifications or masses that may have been overlooked, cancers hiding in the axilla and simulating lymph nodes, linear micro- calcifications simulating vascular calcifications, findings seen on only one mammographic view, and findings at the edge of the film or at the edge of the glandular tissue producing either a tent sign or concavity that was missed at the time of screening.
Of note, most of these cancers were located in the upper outer quadrant, where 50% of all cancers occur. Also, not all the cancers that were missed were small; at least half of the tumors were 1 cm or larger at the time they were missed.
To decrease the number of missed breast cancers, the radi- ologist should use a systematic approach to reviewing the mam- mogram that minimizes distractions, paper shuffling, or other busy work in the reading room at the time of interpretation.
Next, comparison with older films may reveal subtle changes not apparent on only the current examination. Finally, the radi- ologist should be aware of subtle or nonspecific findings of breast cancer.
RCC
Spot
LCC
A
RMLO LMLO
B
C
FIG. 2.36 Spot view workup for a possible mass. Final diagnosis: cancer. (A and B) A mass (arrows) is seen on me- diolateral oblique (MLO; A) craniocaudal (CC; B) screening mammograms in the lower inner portion of the left breast. (C) A spot compression view shows that the density persists and is suggestive of spiculation, representing a mass (arrow). Invasive ductal cancer was diagnosed. R, right; L, left.
B C A
CC
Spot MLO Spot CC
MLO Lateral
D E
F
FIG. 2.37 Importance of using a spot view over an area of fat. (A and B) Craniocaudal (CC; A) and mediolateral oblique (MLO; B) screening mammograms; a possible mass is seen at the inner portion of the left breast on the CC view (arrow) but is not apparent on the MLO view. Incidentally, note the linear metallic scar marker over a skin scar in A. (C) On the lateral view, the mass (arrow) is seen in the upper part of the breast. (D) A spot compression film in the mediolateral view is taken over glandular tissue but shows no mass. (E) When the spot view is repeated over the fatty area on the CC view, it shows a spiculated mass (arrow) in the medial breast against the dark fat that was hidden against the glandular tissue on the mediolateral spot view (D). (F) The specimen shows the hookwire used for preoperative localization and the mass (arrow), which was invasive ductal cancer.
MLO
A B
C D
E
Tomo slice LMLO Tomo slice LCC CC
FIG. 2.38 Tomosynthesis workup for a possible mass. Final diagnosis: cancer. (A and B) Mediolateral oblique (MLO; A) and craniocaudal (CC; B) screening mammograms; a focal asymmetry with possible architectural dis- tortion is seen in the lower outer portion of the left breast (arrows), but the finding is not apparent because of the overlapping fibroglandular tissue. (C and D) Tomosynthesis MLO (C; see Video 2.2A) and CC (D; see Video 2.2B) projections depict the architectural distortion or spiculated mass (circles) clearly, suggesting a malignancy.
(E) Contrast enhanced magnetic resonance image of the left breast shows a spiculated mass, which is proven to be invasive ductal cancer. L, left.
MLO
Tomo slice RMLO Tomo slice RCC
CC
A
C D
B
FIG. 2.39 Tomosynthesis workup for a possible mass. Final diagnosis: cancer. Mediolateral oblique (MLO; A) and craniocaudal (CC; B) screening mammograms; a one-view asymmetry is seen in the outer portion of the right breast (arrow) on CC, but is not seen on MLO. Tomosynthesis MLO (C; see Video 2.3A) and CC (D; see Video 2.3B) projections with photography magnified views on the right depict a spiculated mass (arrows), suggesting a malignancy. This was proven to be invasive ductal cancer. R, right.
MLO
A
C
B
Spot MLO
CC
D E
Tomo slice LMLO Tomo slice LCC
FIG. 2.40 Tomosynthesis workup for a possible mass. Final diagnosis: a summation artifact. (A and B) Medio- lateral oblique (MLO; A) and craniocaudal (CC; B) screening mammograms show a two-view focal asymmetry (arrows) in the upper middle left breast. (C) A possible mass shadow (circle) persists on the spot magnified MLO view. (D and E) Tomosynthesis MLO (D) (see Video 2.4) and CC projections show no mass, but just a breast tissue without a convex margin (arrows). The focal asymmetry was diagnosed as a summation artifact. L, left.
A
MLO
Tomo slice CC Tomo slice Spot CC
CC
B
C D
FIG. 2.41 Tomosynthesis workup for a possible mass. Final diagnosis: a summation artifact. (A and B) Mediolat- eral oblique (MLO; A) and craniocaudal (CC; B) screening mammograms. A one-view asymmetry (arrows) is seen in the inner left breast on the CC view that is not visualized on the MLO view. Because this density has a relatively convex-outward border, further workup was performed to exclude the possibility of malignancy. Please note scar markers on the skin in the bilateral breasts. (C) On tomosynthesis CC (see Video 2.5A) projection, the asymmetry persists (arrow). (D) However, with the use of spot compression, this asymmetry disappeared on the tomosynthe- sis CC projection (see Video 2.5B–C). The asymmetry was diagnosed as a summation artifact.
A
RIGHT BREAST 10:00 8 CM F/NIPP TRANS
2
1+
+ + +
C
RIGHT BREAST 11:00 3 CM F/NIPP TRANS
B
D E
FIG. 2.42 Using markers to correlate mammographic findings with ultrasound. (A) Right MLO mammogram showed a large equal density mass (circle) in the upper right breast. (B and C) Ultrasound showed two large cysts.
(D and E) A right MLO (D) and CC view (E) with BBs (arrows) placed over the cysts seen at ultrasound show that the masses correlate with the cysts.
CC XCCL XCCM
CV
FIG. 2.43 Schematic of variations of the craniocaudal (CC) view to visualize lesions in specific locations. The CC view exaggerated laterally (XCCL) includes outer breast tissue but excludes medial breast tissue. The CC view ex- aggerated medially (XCCM) includes medial breast tissue while excluding outer breast tissue. The cleavage view (CV) includes the medial portions of both breasts on the mammogram. Spot compression may visualize findings close to the chest wall that are excluded by a larger compression paddle.
Cleopatra view
FIG. 2.45 Cleopatra view. For this view the patient leans outward and back, essentially performing an outer cra- niocaudal view exaggerated laterally with a degree of obliquity to image more outer tissue.
A
MLO
Spot MLO
CC XCCL
B C
D
FIG. 2.44 Craniocaudal view exaggerated laterally (XCCL). (A and B) Mediolateral oblique (MLO; A) and craniocaudal (CC; B) screening mammograms. There is a round mass with a marker on it in the upper left breast on the MLO view that is not seen on the CC view, even though the marker shows the palpable mass. (C) An XCCL now shows the mass by including it in the field of view. (D) A spot compression MLO view shows the mass, and it is invasive ductal cancer.
A
MLO CC XCCM
B C
FIG. 2.46 Craniocaudal view exaggerated medially (XCCM). (A) A left mediolateral oblique (MLO) view shows the mass (arrow) deep in the upper breast at the chest wall. (B) However, the left craniocaudal (CC) view shows no mass. (C) XCCM successfully shows a small mass (arrow) in the medial portion of the breast. This was proven to be invasive ductal cancer. Note that there are two ribbon markers in the outer right breast tissue.
B A
MLO CC CV
C
FIG. 2.47 Cleavage view (CV) mammogram that shows more of the inner breast. (A and B) Mediolateral oblique (MLO; A) and craniocaudal (CC; B) screening mammograms show a calcified degenerating fibroadenoma (ar- rows) in the middle inner left breast. (C) The CV mammogram shows the fibroadenoma in the inner breast to the best advantage and also includes some of the inner portion of the contralateral breast. Incidentally, note the linear metallic scar marker over skin scars in A–C.
A B C
FIG. 2.48 Methods to visualize high breast lesions. (A) The compression paddle may exclude high breast masses by compressing them out of the field of view. (B) A view with the cassette holder above the nipple to allow com- pression of only the upper breast tissue. (C) The right image shows a from-below (FB) view in which the image receptor is placed over the upper part of the breast and the compression paddle approaches the receptor from the lower part of the breast. (Modified from Sickles EA: Practical solutions to common mammographic problems:
tailoring the examination, AJR Am J Roentgenol 151:31–39, 1988.)
A
CC Spot
B
FIG. 2.49 Spot view showing a mass in the retroareolar region. (A) A craniocaudal (CC) view shows a vague den- sity behind the nipple, but the nipple is not in profile. (B) A spot view with the nipple in profile shows a spiculated mass that was diagnosed as invasive lobular cancer.
A LIQ lesion SIO
Axilla Axilla
B
FIG. 2.50 Superior–inferior oblique (SIO) view. (A) Schematic shows a lower inner quadrant (LIQ) lesion in the left image. The SIO view is obtained with the image receptor next to the inner breast lesion and the compression plate compressing from the superior axillary side. (B) Model demonstrating positioning for the SIO view.
A
MLO
Lumpogram
CC
B
C D
FIG. 2.51 Spot compression over a palpable mass (the lumpogram). (A and B) Mediolateral oblique (MLO; A) and craniocaudal (CC; B) views show no defined mass at the 3 o’clock position on the right breast with the pal- pable abnormality. Note a BB skin marker (A; arrowhead) placed at the palpable portion. (C) Spot tangential view over the lump with the BB marker (arrowhead) in the CC projection shows a possible round mass (arrows) against the dense tissue. (D) Ultrasound shows an oval smooth mass, representing a fibroadenoma on biopsy.
BOX 2.8 Mammographic Views to Characterize a True Lesion
Magnification
Spot compression magnification Tomosynthesis
B A
MLO
Spot Mag MLO Spot Mag CC
CC
D C
E
E F
FIG. 2.52 Use of magnification views. (A and B) Mediolateral oblique (MLO; A) and craniocaudal (CC; B) mam- mograms show a spiculated mass (arrows), which is seen better on the CC view than on the MLO view. Distor- tion and the tent sign are evident in the upper part of the breast. (C and D) Spot magnification views show the spiculated mass to better advantage on both the MLO (C) and CC (D) views. (E) Ultrasound shows an oval (a very hypoechoic mass that has no acoustic spiculation or shadowing) corresponding to the mass on the mammo- gram. (F) The mass was localized by ultrasound and was removed, as shown by the specimen. Note the localizing hookwire. Invasive ductal cancer was the diagnosis.
MLO
Tomo slice RMLO Tomo slice RCC
CC
A
C D
B
FIG. 2.53 Tomosynthesis to characterize a true finding in extremely dense breasts. (A and B) Mediolateral oblique (MLO; A) and craniocaudal (CC; B) projections of tomosynthesis-synthesized 2D mammograms show a possible mass (arrows) below the BB skin marker in the right upper outer breast. However, its margin is largely obscured by the overlapped dense fibroglandular tissue. (C and D) Tomosynthesis slices depict the spiculated margin better on both MLO (C; see also Video 2.6A) and CC (D) (see also Video 2.6B) projections. On tomosynthesis slices, the mass appears more dense and more homogenous compared with the surrounding fibroglandular tissue that has heterogeneous density caused by marbled fat tissue. Invasive ductal cancer was the diagnosis. R, right.
TABLE 2.9 Reasons for Missed Cancers Errors in technique Poor technique
Poor positioning
Cancer in location not included in standard field of view
Errors in detection “Overlooked, missed”: characteristic cancer findings, present in retrospect;
this commonly occurs particularly in tumors with morphology that is similar to background fibroglandular tissue displayed on mammography
“Unrecognized sign”: atypical finding perceived but not acted on, such as round mass or developing focal asymmetry
“Nonspecific findings” that look normal (not actionable, not an error)
Errors in
interpretation Radiologist sees and perceives finding, incorrectly interprets finding as nonactionable
True negative study Tumor cannot be seen even in retrospect From Ikeda DM, Andersson I, Wattsgard C, et al: Interval carcinomas in the Malmö Mammographic Screening Trial: Radiographic appearance and prognostic consider- ations, AJR Am J Roentgenol 159:287–294, 1992.
BOX 2.9 Types of Findings on Mammograms in Patients with Missed Breast Cancer
Occult on mammography (negative)
Nonspecific findings (normal or benign findings) Atypical findings (subtle)
Classic cancer findings overlooked or misinterpreted
From: Ikeda DM, Andersson I, Wattsgard C, et al: Interval carcinomas in the Malmö Mammographic Screening Trial: Radiographic appearance and prognostic consider- ations, AJR Am J Roentgenol 159:287–294, 1992.
BOX 2.10 Features of Cancer Missed on Previous Mammography
Lesion seen on only one view Distracting lesions
Radiolucent lines of fat through the lesion Too few calcifications
Small masses
Calcifications look like calcifying blood vessel Lesion in dense breast tissue
Lesion at the edge of glandular tissue Lesion at the edge of the film
Lesion in the axilla that looks like a lymph node Benign-appearing lesion
Lesion in large breast
Lesion obscured by a blood vessel
Lesion on mammography with suboptimal technique Lesion outside the image
From: Birdwell RL, Ikeda DM, O’Shaughnessy KF, Sickles EA: Mammographic char- acteristics of 115 missed cancers later detected with screening mammography and the potential utility of computer-aided detection, Radiology 219:192–202, 2001.
Key Elements
Breast cancer screening in women invited to undergo mam- mography decreases breast cancer mortality by about 30%.
Risk factors for breast cancer include age older than 50 years, personal history of or first-degree relative with breast can- cer, nulliparous status, early menarche, late menopause, first birth after age 30, radiation treatment, atypical duc- tal hyperplasia, lobular carcinoma in situ, and presence of BRCA1 or BRCA2 breast cancer susceptibility genes.
Seventy percent of women who have breast cancer have no risk factors other than being female and being older than age 50.
Signs and symptoms of breast cancer include a breast lump, bloody or new spontaneous nipple discharge, new nipple or skin retraction, peau d’orange, and symptoms from metastasis.
Signs of breast cancer on mammography include a spicu- lated mass, pleomorphic calcifications, a round mass, ar- chitectural distortion, a developing density, an asymmet- ric density, a single dilated duct, lymphadenopathy, and breast edema; in some patients, no mammographic signs are present (occult cancer).
A normal mammogram is dense in young women and becomes darker over time as the dense tissue is replaced by fat.
Increasing breast density may be caused by pregnancy or hormone replacement therapy.
Unexplained increasing breast density should prompt a work- up to exclude breast edema or cancer.
Evaluation of a normal mammogram includes routine inspec- tion for fibroglandular symmetry and examination of the periglandular edges, the skin, retroareolar region and nipple, retroglandular fat, medial part of the breast, chest wall, and axilla.
Normal asymmetric glandular tissue occurs in 3% of women and looks like an asymmetry of normal glandular tissue without a palpable mass, suspicious calcifications or spicu- lations, a three-dimensional mass, or new findings.
Be alert for findings in the medial part of the breast; the nor- mal sternalis muscle variant is the one normal finding in the medial breast.
To detect developing densities, change, or asymmetries, view films back to back and compare them with old films.
Review both the breast history and the technologist’s physi- cal sheet before interpretation of the mammogram to know where previous biopsies were, the meaning of skin markers, and to be aware of patient complaints.
Women with breast cancer have normal mammograms 10%
to 15% of the time.
The skin should normally be 2 to 3 mm thick. Skin thicker than 2 to 3 mm might be breast edema or scarring.
Special mammographic views confirm or exclude ques- tionable findings seen on screening mammography, characterize true lesions, and triangulate the location of a lesion.
Rolled views, compression views, and step oblique views dis- tinguish true lesions from summation artifacts.
Magnification spot compression views characterize mass mar- gins and shapes and see calcification numbers, shapes, and forms better.
Air-gap magnification views resolve the shape and number of calcifications better than standard mammograms.
Laterally exaggerated craniocaudal (CC) and Cleopatra views display the outer part of the breast.
Medially exaggerated CC and cleavage views display the in- ner portion of the breast.
From-below and upper breast views display the upper part of the breast.
Spot compression and nipple-in-profile images view the nip- ple and retroareolar region.
Superior–inferior oblique views (reverse oblique) display the lower inner portion of the breast.
The breast location most often excluded by screening mam- mograms is the upper inner quadrant.
Lesions displayed at the nipple level on the mediolateral oblique (MLO) view may be in the upper, lower, or mid- portion of the breast on the ML view.
Triangulation with the CC and MLO views can be used to predict the location of the lesion on the lateral view.
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