Missed Cancers Lessons
Missed Cancers Lessons
Missed Cancers Lessons
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Missed Breast Carcino-
ma: Pitfalls and Pearls1
Aneesa S. Majid, MD ● Ellen Shaw de Paredes, MD ● Richard D.
Doherty, MD ● Neil R. Sharma ● Xavier Salvador
Index terms: Breast neoplasms, 00.32 ● Breast neoplasms, radiography, 00.11 ● Diagnostic radiology, observer performance
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Figure 1. Invasive ductal carcinoma in a 36-year-old woman with dense breasts and a pal-
pable mass. (a) Left mediolateral oblique mammogram demonstrates no finding that corre-
sponds to a palpable mass (arrow). (b) US image obtained in the area of the palpable abnor-
mality reveals a heterogeneous, hypoechoic mass with irregular margins. Although there is
no acoustic shadowing and the mass is wider than it is tall, the hypoechogenicity and irregu-
lar margins are suspect for malignancy. Pathologic analysis demonstrated invasive ductal car-
cinoma.
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Figure 3. Proper positioning. (a) Left mediolateral oblique (left) and craniocaudal (right) mam-
mograms obtained with improper positioning demonstrate poor visualization of the posterior tis-
sue. The margin of a mass is barely perceptible at the edge of the mediolateral oblique image (ar-
row). (b) On a left mediolateral oblique mammogram obtained with improved positioning, a can-
cer is seen near the chest wall. An exaggerated craniocaudal view may also help demonstrate such a
mass.
be 99.8% and 100%, respectively. Moy et al (11) rant, which demonstrates the greatest proportion
found the negative predictive value of US with of breast cancers, is necessary. However, the tech-
mammography for a palpable mass to be 97.4%. nologist must use the craniocaudal view as a
However, a palpable mass that appears solid at complement to the mediolateral oblique view to
US warrants further evaluation with biopsy. visualize the medial tissue as well.
Creative positioning may be necessary to in-
Poor Positioning clude areas of palpable abnormalities on the im-
Proper positioning and image contrast are abso- ages. Radiopaque markers should be placed on
lutely necessary in all aspects of radiology, but palpable areas, with repositioning of the marker
especially in mammography. The technologist between projections as needed to keep the marker
must adhere to the positioning standards to maxi- superimposed on the palpable finding. In addi-
mize the amount of tissue included on the image tion, a spot compression view obtained over a
(12). Findings on the mediolateral oblique view palpable mass with the skin in tangent can reveal
that indicate proper positioning include visualiza- an underlying mass and demonstrate overlying
tion of the pectoralis muscle to the level of the skin thickening or retraction. Creative positioning
nipple, a convex appearance of the pectoralis ma- may also be helpful in patients who are tense, who
jor muscle, complete visualization of posterior have suffered a stroke, or who have shoulder
breast tissue, breast tissue that is well compressed problems or other debilitating factors that limit
and positioned in an up-and-out orientation, and visualization of the posterior breast on standard
an open inframammary fold (Fig 3). At cranio- mediolateral oblique views.
caudal imaging, the technologist should verify Off-angle or step oblique views are very helpful
that the breast is pulled straight forward and not in the evaluation of densities or abnormalities
exaggerated laterally, and that the breast tissue is seen in only one projection (13). Densities seen
well compressed. The difference between the pos- on the craniocaudal view alone may be further
terior nipple line measurement on the mediolat- characterized and localized with use of spot com-
eral oblique and craniocaudal views should not pression and rolled craniocaudal views. If a lesion
exceed 1 cm. Emphasis on the upper outer quad- rolls medially when the top of the breast is rolled
medially, it is located superiorly; if it rolls later-
ally, it is located inferiorly. The technologist
should label the image with the orientation in
RG f Volume 23 ● Number 4 Majid et al 885
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which the top of the breast was rolled (eg, cranio- be helpful in verifying the location of a mass that
caudal RL ⫽ “craniocaudal rolled laterally”). If a is clearly seen on only one view.
density is seen only on the mediolateral oblique
view, a mediolateral view is required to locate and Poor Technique
further evaluate the lesion (Fig 4). In such a case, The technologist must optimize image contrast to
a medial lesion will move superiorly on the lateral avoid obtaining over- or underpenetrated images.
view, whereas a lateral lesion will move inferiorly. Proper positioning of the photocell is necessary
This concept of triangulation is extremely impor- to achieve correct optical density on the image.
tant in identifying the actual position of a lesion. Careful attention to daily processor quality con-
Off-angle or step oblique views, like standard trol is also necessary to optimize contrast. The
views, are most helpful when the lesion is super- technologist should always review the images
imposed over fat and not dense tissue. Exagger-
ated craniocaudal views may be helpful in demon-
strating a posteriorly located lesion that is seen on
the mediolateral oblique view only. US may also
886 July-August 2003 RG f Volume 23 ● Number 4
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under proper mammographic viewing conditions curs when the lesion is included in the field of
to assess the adequacy of imaging technique (Fig view and is evident but is not recognized by the
5). Image blur is problematic, particularly in the radiologist. The lesion may or may not have
assessment of microcalcifications. Rosen et al subtle features of malignancy that cause it to be
(14) found that in 62% of cancers that manifested less visible. Small nonspiculated masses, areas of
as microcalcifications and were incorrectly fol- architectural distortion and asymmetry, and small
lowed up with imaging rather than biopsy, image clusters of amorphous or faint microcalcifications
blur on magnification views compromised image may all be difficult to perceive.
quality. To avoid perception error, images should be
reviewed as mirror images, with mediolateral
Lack of Perception oblique images placed together and craniocaudal
Two major causes of missed breast cancers are images placed together (Figs 6, 7). The radiolo-
related to radiologist error. The first of these gist should compare like areas on the side-by-side
causes is lack of perception. Perception error oc- images to identify any focal asymmetric density or
low-density mass. Identification of a focal density
should prompt a search for this density on the
corresponding view in the same arc from the
RG f Volume 23 ● Number 4 Majid et al 887
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Figure 10. Satisfaction of search. Right mediolateral oblique (a) and craniocaudal (b) mammo-
grams demonstrate subtle architectural distortion (arrow) behind an obvious calcified fibroad-
enoma. The first interpreting radiologist noted the fibroadenoma but missed the distortion, which
proved to be invasive ductal carcinoma.
nipple (Fig 8). Additional views may be needed to of patients (15) and may actually be seen in 9%–
verify the presence of a true lesion. 10% of patients at MR imaging (16). Satisfaction
Failure to diagnose multifocal and multicentric of search can also occur in cases of an obvious
breast cancers can directly affect patient treat- benign lesion with a subtle cancer. The radiolo-
ment. Multifocal breast cancer is defined as two gist must not be satisfied with finding just one
or more cancers in the same quadrant, whereas lesion, but must search carefully for others,
multicentric breast cancer is defined as two or whether benign or malignant.
more cancers in different quadrants (Fig 9). In Another special circumstance that can present
multicentric disease, breast conservation therapy a perception problem involves a patient with a
is contraindicated. These disease entities may not palpable node in the axilla that is evaluated with
be perceived owing to “satisfaction of search,” in biopsy and represents metastatic adenocarci-
which observation of an obvious finding misleads noma, likely of breast origin. The primary breast
the radiologist into not looking carefully for other cancer may be occult and either not observed or
lesions (Fig 10). Careful attention must also be very subtle at mammography. Careful attention
paid to the contralateral breast after observation
of a suspect lesion because contralateral synchro-
nous cancers have been reported in 0.19%–2.0%
890 July-August 2003 RG f Volume 23 ● Number 4
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Figure 11. Occult cancer with metastases in a 36-year-old woman. (a) Right mediolateral oblique mammo-
gram that was thought to be otherwise negative reveals an enlarged axillary node (arrow) that was palpable.
(b) On a right mediolateral oblique mammogram obtained 3 months later while the patient was being evalu-
ated for adenopathy, the previously occult cancer in the 11 o’clock position (arrowhead) became visible. Patho-
logic analysis demonstrated invasive ductal carcinoma with metastasis to the axilla.
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Figure 12. Apparent lesion thinning at spot compression mammography. (a, b) Right craniocaudal (a) and
mediolateral oblique (b) mammograms demonstrate focal architectural distortion (arrow in a) that may corre-
spond to a superiorly located lesion (arrowhead in b). (c, d) Mediolateral oblique (c) and craniocaudal (d)
spot compression mammograms show a persistent but less prominent area of distortion. At 6-month follow-up
mammography, the area appeared more prominent, and biopsy was performed. Pathologic analysis demon-
strated invasive ductal carcinoma. Rolled craniocaudal views were also obtained and helped confirm the persis-
tence of the lesion.
892 July-August 2003 RG f Volume 23 ● Number 4
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Figure 14. Asymmetric density. Bilateral mediolateral oblique (a) and craniocaudal (b) mammograms demon-
strate a new focal asymmetric area in the left axillary tail (arrow), a finding that becomes more evident with mirror
image interpretation. Biopsy revealed infiltrating lobular carcinoma.
RadioGraphics suggest malignancy but that has been stable for radiologist should take the following steps when
1–2 years still requires biopsy because it may rep- interpreting mammographic findings:
resent a slowly changing cancer. In particular, 1. Do not rely on screening views alone to di-
caution should be used in evaluating stable agnose a detected abnormality; complete the
masses or lesions with suspect morphologic fea- evaluation with diagnostic mammography.
tures that decrease in size in patients who are re- 2. Review clinical data and use US to help as-
ceiving tamoxifen. Tamoxifen is used to treat sess a palpable or mammographically detected
breast cancers and to prevent the development of mass.
breast cancer in high-risk women, but it can also 3. Be strict about positioning and technical
be used to check the growth of occult malignan- requirements to optimize image quality.
cies. 4. Be alert to subtle features of breast cancers.
5. Compare current images with multiple
Role of Double Reading prior studies to look for subtle increases in lesion
Double reading of mammograms has been shown size.
to increase the detection rate for breast cancer by 6. Look for other lesions when one abnormal-
up to 15% (29,30). Computer-aided detection ity is seen.
(CAD) represents a relatively new technology 7. Judge a lesion by its most malignant fea-
that has been implemented in some mammogra- tures.
phy facilities for double reading. Clinical studies
have shown that CAD increases the sensitivity of Acknowledgment: The authors wish to thank Louise
Logan for manuscript preparation.
breast cancer detection by radiologists by up to
20% (31,32). The sensitivity of the CAD systems
is greater for detecting calcifications than for de-
References
1. Baker LH. Breast Cancer Detection Demonstra-
tecting masses (33). In a study of 115 cancers tion Project: five-year summary report. CA Cancer
retrospectively judged to merit recall on the J Clin 1982; 32:194 –225.
screening mammogram prior to the mammogram 2. Harvey JA, Fajardo LL, Innis CA. Preview mam-
on which they were diagnosed, 77% of lesions mograms on patients with impalpable breast carci-
were identified with CAD (34). In all, 86% of 35 nomas: retrospective vs blind interpretation. AJR
Am J Roentgenol 1993; 161:1167–1172.
missed areas of calcifications and 73% of 80 3. Elmore JG, Wells CK, Lee CH, et al. Variability in
missed malignant masses were detected with radiologists’ interpretations of mammograms.
CAD. We may continue to see increasing use of N Engl J Med 1994; 331:1493–1499.
both CAD and a second radiologist for double 4. Patel MR, Whitman GJ. Negative mammograms
reading of screening mammograms. in symptomatic patients with breast cancer. Acad
Radiol 1998; 5:26 –33.
5. Burrell HC, Sibbering DM, Wilson AR, et al.
Conclusions Screening interval breast cancers: mammographic
Although mammography is the standard of refer- features and prognosis factors. Radiology 1996;
ence for the detection of early breast cancer, as 199:811– 817.
many as 30% of breast cancers may be missed. 6. Bird RE, Wallace TW, Yankaskas BC. Analysis of
cancers missed at screening mammography. Radi-
To reduce the possibility of missing a cancer, the ology 1992; 184:613– 617.
7. Goergen SK, Evans J, Colen GPB, Macmillan JH.
Characteristics of breast carcinomas missed by
radiologist. Radiology 1997; 204:131–135.
RG f Volume 23 ● Number 4 Majid et al 895
RadioGraphics 8. Ikeda DM, Andersson I, Wattsgard C, et al. Inter- 22. Swann CA, Kopans DB, Koerner FC, McCarthy
val carcinomas in the Malmo Mammographic KA, White G, Hall DA. The halo sign and malig-
Screening Trial: radiologic appearance and prog- nant breast lesions. AJR Am J Roentgenol 1987;
nostic considerations. AJR Am J Roentgenol 1992; 149:1145–1147.
159:287–294. 23. Stavros AT, Thickman D, Rapp CL, et al. Solid
9. Soo MS, Rosen EL, Baker JA, et al. Negative pre- breast nodules: use of sonography to distinguish
dictive value of sonography with mammography in between benign and malignant lesions. Radiology
patients with palpable breast lesions. AJR Am J 1995; 196:123–124.
Roentgenol 2001; 177:1167–1170. 24. Sickles EA. Nonpalpable circumscribed noncalci-
10. Skaane P. Ultrasonography as adjunct to mam- fied solid breast masses: likelihood of malignancy
mography in the evaluation of breast tumors. Acta based on lesion size and age of patient. Radiology
Radiol 1999; 420(suppl):1– 47. 1994; 192:439 – 442.
11. Moy L, Slanetz P, Moore R, et al. Specificity of 25. Mendelson EB, Harris KM, Doshi N, Tobon H.
mammography and ultrasound in the evaluation of Infiltrating lobular carcinoma: mammographic
a palpable abnormality: retrospective review. Radi- patterns with pathologic correlation. AJR Am J
ology 2002; 225:176 –181. Roentgenol 1989; 153:265–271.
12. Hendrick RE, Bassett L, Botsco MA, et al. Mam- 26. Huynh PT, Parellada JA, Shaw de Paredes E, et
mography quality control manual. Reston, Va: al. Dilated duct pattern at mammography. Radiol-
American College of Radiology, 1999. ogy 1997; 204:137–141.
13. Pearson K, Sickles E, Frakel S. Efficacy of step- 27. Fournier DV, Weber E, Hoeffken W, et al.
oblique mammography for confirmation and local- Growth rate of 147 mammary carcinomas. Cancer
ization of densities seen on only one standard 1980; 45:2198 –2207.
mammographic view. AJR Am J Roentgenol 2000; 28. Lev-Toaff AS, Feig SA, Saitas VL, et al. Stability
174:745–752. of malignant breast microcalcifications. Radiology
14. Rosen EL, Baker JA, Soo MS. Malignant lesions 1994; 198:153–156.
initially subjected to short-term mammographic 29. Anderson ED, Muir BB, Walsh JS, et al. The effi-
follow-up. Radiology 2002; 223:221–228. cacy of double reading mammograms in breast
15. Kinne DW. Management of the contralateral screening. Clin Radiol 1994; 49:248 –251.
breast. In: Harris JR, Hellman S, Henderson P, et 30. Thurjell EL, Lernevall KA, Taube AAS. Benefit of
al, eds. Breast diseases. Philadelphia, Pa: Lippin- independent double reading in a population-based
cott, 1987; 620 – 621. mammography screening program. Radiology
16. Liberman L, Morris E, Kim C, et al. MR imaging 1994; 191:241–244.
findings in the contralateral breast in women with 31. Burhenne LJ, Wood SA, D’Orsi CJ, et al. Poten-
recently diagnosed breast cancer. AJR Am J tial contribution of computer-aided detection to
Roentgenol 2003; 180:333–341. the sensitivity of screening mammography. Radiol-
17. Orel S, Weinstein SP, Schnall MD, et al. Breast ogy 2001; 56:150 –154.
MR imaging in patients with axillary node metas- 32. Brem RF, Schoonjans JM. Radiologists detection
tases and unknown primary malignancy. Radiol- of microcalcifications with and without computer-
ogy 1999; 212:543–549. aided detection: a comparative study. Clin Radiol
18. Khalkhali I, Vargas HI. The role of nuclear medi- 2001; 56:150 –154.
cine in breast cancer detection: functional breast 33. Lechner M, Nelson M, Elvecrog E. Comparison of
imaging. Radiol Clin North Am 2001; 39:1053– two commercially available computer-aided detec-
1068. tion (CAD) systems. Appl Radiol 2002; 31:31–35.
19. Orel SG. MR imaging of the breast. Radiol Clin 34. Birdwell RL, Ikeda DM, O’Shaugnessy KF, Sick-
North Am 2000; 38:899 –913. les EA. Mammographic characteristics of 115
20. Berg WA, Gilbreath PL. Multicentric and multifo- missed cancers later detected with screening mam-
cal cancer: whole breast ultrasound in preoperative mography and the potential utility of computer-
evaluation. Radiology 2000; 214:59 – 66. aided detection. Radiology 2001; 219:192–202.
21. Sickles EA. Mammographic features of 300 con-
secutive nonpalpable breast cancers. AJR Am J
Roentgenol 1986; 146:661– 663.