Breast Cancer Risk Factors

Risk factors for breast cancer are important to consider when reading mammograms, because they indicate a pretest probability of breast cancer. Compiling risk information on the breast history sheet provides the interpreting radiologist quick and easy-to-use access to this information (Fig. 2-1). Breast cancer risk factors are listed in Box 2-1. The most important risk factors are older age and female gender; U.S. statistics indicate that breast cancer will develop in one in eight women, if the women have a 90-year life span. Men also develop breast cancer, but only 1% of all breast cancers occur in men.

The risk for breast cancer increases with increasing age and drops off at age 80. Women with a personal history of breast cancer have a higher risk of developing breast cancer in the ipsilateral or contralateral breast than does the general population. In women undergoing breast conservation, the conservatively treated breast has a 1% per year risk of developing cancer.

A family history of breast or ovarian cancer is a particularly important risk factor. The age, number, and cancer type in the affected relative is especially significant. Women with a first-degree relative (mother, daughter, or sister) with breast cancer have about double the risk of the general population and are at particularly high risk if that cancer was premenopausal or bilateral. If many relatives had breast or ovarian cancer, the woman may be a carrier of BRCA1 or BRCA2, the autosomal dominant breast cancer susceptibility genes. Genetic testing for these genes is possible. However, genetic testing is most appropriate when combined with the counseling, evaluation, and support provided by a genetic screening center because of the untoward social effects of positive (or negative) results. Carriers of the breast cancer susceptibility gene BRCA1 on chromosome 17 have a breast cancer risk of 85% and an ovarian cancer risk of 63% by age 70. Women with BRCA2 on chromosome 15 have a high risk of breast cancer and a low risk of ovarian cancer. These genes account for 5% of all breast cancers in the United States and for 25% of breast cancers in women younger than age 30. Women of Ashkenazi (Eastern European) Jewish heritage have a slightly higher risk of breast cancer than does the general population (Box 2-2), but additional work is being done to determine whether this population has a higher rate of breast and ovarian cancer related to BRCA1 and BRCA2 mutations. Other genetic syndromes that have a higher risk of breast cancer include the Li-Fraumeni, Cowden, and ataxia-telangiectasia syndromes.

Early menarche (before age 12), late menopause (after age 55), nulliparity, and first live birth after age 30 bestow a slightly higher risk for breast cancer, as a result of having more menstrual cycles and longer exposure to estrogen and progesterone. Data from a 2003 study, part of the Women’s Health Initiative, a randomized, controlled trial of the effects of estrogen plus progestin (combination hormone replacement therapy [CHRT]) versus placebo, showed a 24% greater incidence of breast cancer in women receiving CHRT versus the control group. Whereas previous data showed an adjusted relative risk of 1.46 for the development of breast cancer in women receiving CHRT for more than 5 years, the 2003 analysis showed the risk for breast cancer rising within 5 years of starting CHRT; in addition, it showed more difficulty in detecting cancers by mammography in this group.

A breast biopsy showing atypical ductal hyperplasia (ADH) histology increases the risk for breast cancer to four to five times that of the general population. The presence of lobular carcinoma in situ (LCIS) also increases the risk for breast cancer, but at a much higher rate than ADH, about 10 times that of the normal population. LCIS is a misnomer and not a cancer at all. Rather, LCIS is a high-risk marker for developing breast cancer. A woman with LCIS has a 27% to 30% chance of developing invasive ductal or lobular cancer in the ipsilateral or contralateral breast over a 10-year period. Thus, a biopsy showing LCIS results in patient management of either “watchful waiting” with increased surveillance by frequent imaging and physical examination, or bilateral mastectomy.

Women who had an early exposure to radiation also have an increased risk for breast cancer. A medical history of radiation therapy for Hodgkin disease, multiple fluoroscopic examinations for tuberculosis, ablation of the thymus, or treatment of acne with radiation infers possible scattered radiation to the breasts, which may induce breast cancer. In fact, the risk for developing breast cancer is so high in women with Hodgkin disease that in 2008 the American Cancer Society recommended magnetic resonance screening for Hodgkin’s disease survivors.

Extensive mammographic breast density, or a large amount of fibroglandular tissue within the breast by volume as measured on the mammogram, is strongly associated with the risk of breast cancer. However, the association and the reasons for this finding, as well as its relative association among different ethnicities, are still being studied.

Other lifestyle choices also affect breast cancer risk. One is drinking alcohol. One drink per day bestows a very small risk, but two to five drinks per day increases the risk to 15 times that of women who do not drink. Being overweight or obese also increases the risk of cancer, especially if the weight gain happens after menopause and the fat is around the abdomen. A woman with an “apple-shaped” body is at higher risk than one with a “pear-shaped” body. Exercise has been shown to reduce breast cancer risk after menopause, with one study suggesting that cancer risk was reduced at least in part via hormonal pathways. However, more study of these changeable risk factors is needed.

Quantitative statistical models that estimate the short-term or lifetime risk for breast cancer include the Claus model and the Gail statistical model. These models compile individual risk factors and combine them into an estimate of the lifetime risk for breast cancer for individual women.

Despite all these risk factors, it remains true that 70% of all women with breast cancer have none of these risk factors other than older age and female gender.

Signs and Symptoms of Breast Cancer

Women, or their partners, often find their own breast cancer by discovering a palpable hard breast lump. Breast lumps are a common symptom for which women seek advice (Box 2-3). Of particular concern are new, growing, or hard breast masses. Masses that are stuck to the skin or chest wall are particularly worrisome for an invasive breast cancer.

Nipple discharge is another finding for which women often seek advice. Nipple discharge is usually benign, especially if it is whitish, green, or yellow and is produced from several ducts. Nipple discharge is suspicious for cancer if it is new, expressed from only one duct, bloody or serosanguineous, spontaneous, copious, or serous. An example of a suspicious history is a woman finding new bloody or serous nipple discharge on her nightgown or undergarments.

Nipple inversion is a sign of breast cancer if it is new. Longstanding nipple inversion is not uncommon, however; inverted nipples may be present at birth and are benign. On the other hand, new nipple inversion is of concern because a retroareolar tumor can produce nipple retraction.

Similarly, skin retraction or dimpling is a sign of breast cancer, due to tethering of the skin by cancer. On physical examination, skin retraction or tethering may be seen with the patient’s arms at her sides when she inspects her breasts in the mirror. Raising the patient’s arms or placing her hands on her hips pulls in the pectoralis muscle and may show skin tethering under the breasts that was previously invisible or may make the tethering more apparent.

Peau d’orange is a physical finding indicating breast edema; it is caused by skin edema rising around the bases of tethered hair follicles, resulting in skin pitting, or “orange peel” skin. Breast edema is a nonspecific finding and may indicate inflammatory cancer, mastitis, or axillary lymph node obstruction.

Despite all these signs and symptoms of breast cancer, some women have no physical findings or symptoms at all despite having breast cancer. Their breast cancers are detected on screening mammography.

Breast pain is not generally caused by cancer, but it deserves mention because it is a common cause of morbidity. If cyclic, breast pain is usually endocrine in nature. Although breast pain is usually due to benign etiologies, unfortunately, both breast pain and breast cancer are common. Thus, the physician’s goals are to reassure patients with breast pain, search for treatable causes of breast pain such as cysts, and exclude coexistent malignancy.

The Normal Mammogram

A normal breast is composed of a honeycomb supporting fibrous structure made up of Cooper ligaments that houses fatty tissue, which in turn supports the glandular elements of the breast (Fig. 2-2A). The glandular elements are composed of lactiferous ducts leading from the nipple and branching into excretory ducts, interlobular ducts, and terminal ducts leading to the acini that produce milk. The ducts are lined throughout their course by epithelium composed of an outer myoepithelial layer of cells and an inner secretory cell layer. The ducts and glandular tissue extend posteriorly in a fanlike distribution consisting of 15 to 20 lobes draining each of the lactiferous ducts, with most of the dense tissue found in the upper outer quadrant. Posterior to the glandular tissue is retroglandular fat, described by Dr. Laszlo Tabar as a “no man’s land,” in which no glandular tissue should be seen. The pectoralis muscle lies behind the fat on top of the chest wall.

On the normal mediolateral oblique (MLO) mammogram, the pectoralis muscle is a concave structure posterior to the retroglandular fat near the chest wall. Normal lymph nodes high in the axilla overlie the pectoralis muscle (see Fig. 2-2B and C). Normal lymph nodes are sharply marginated, oval, or lobulated dense masses with a radiolucent fatty hilum. They are commonly found in the upper outer quadrant of the breast along blood vessels. Lymph nodes also occur normally within the breast and are known as normal “intramammary” lymph nodes. If the lymph node has the typical kidney bean shape and a fatty hilum, it should be left alone. If one is uncertain about whether a mass represents an intramammary lymph node, mammographic magnification views may help display the fatty hilum, or ultrasound may show the typical hypoechoic appearance of the lymph node and the echogenic fatty hilum.

Usually fibroglandular tissue occurs symmetrically in the upper outer quadrants of the breasts. The breast tissue is usually distributed fairly symmetrically from left to right. When viewing mammograms, the clinician should place the mammograms back to back so that the chest walls face each other for easy viewing of tissue symmetry (see Fig. 2-5A). Fatty tissue surrounds the glandular tissue.

On the normal craniocaudal (CC) projection, the pectoralis muscle produces a half-moon–shaped density near the chest wall (Fig. 2-3A and B). Fat lies anterior to the muscle, and the white glandular tissue lies anterior to the fat. In older women, most of the glandular tissue in the medial breast undergoes fatty involution, and therefore most of the residual dense glandular tissue exists in the upper outer breast.

There should be only fatty tissue in the medial breast near the chest wall. The only normal exception is the sternalis muscle, a muscular density near the medial aspect of the chest wall that should not be mistaken for a mass (see Fig. 2-3C and D). If there is a question that the density is a mass instead of the sternalis muscle, a cleavage view (CV) mammogram or ultrasound can prove that the density is a muscle and a normal structure.

Breast “density” is an important feature of the mammogram that describes how much of the breast is filled with glandular tissue, which looks white on the mammogram. Fat is black on the mammogram. Women normally have varying ratios of glandular and fatty tissue in their breasts. A “dense” mammogram has very glandular breast tissue in it and looks mostly white. The opposite of a “dense” mammogram is a “fatty” mammogram, which looks mostly black. Because breast cancer is also white on the mammogram, a white “dense” normal background of glandular tissue can hide a cancer, just like a polar bear can hide in a snowstorm.

The American College of Radiology’s (ACR) Breast Imaging Reporting and Data System (BI-RADS®) lexicon separates breast density into quartiles depending on how much glandular tissue the breast contains by volume. “Dense” contains the most white (>75% dense), “heterogeneously dense” is less white (50–75% dense), “scattered fibroglandular” is even less white (25–50%), and “fatty” is the least white (<25% dense) (Box 2-4). A “dense” breast does not mean the breast is hard to the touch. Breast density has little correlation to how hard or soft the breast feels on physical examination; that is, you cannot predict how soft a breast will feel by looking at the mammogram. Radiologists describe breast density in the mammogram report so that referring doctors will know how white the breast looks and how confident the radiologist is in excluding cancer.

Young women have mostly glandular breasts, and their mammograms are described as “dense.” As women age, the fibroglandular tissue involutes into fat, which is black. The natural progression of the mammogram is mostly white (dense) at a young age when the breasts are filled with glandular tissue, becoming progressively darker as the woman ages and her glandular tissue turns into fat. The amount of remaining glandular tissue varies from woman to woman. Some older women have surprisingly large amounts of dense white tissue on the mammogram; the amount remaining depends on genetics, parity, and exogenous hormone replacement therapy. But generally as women age, the glandular tissue involutes so that there are relatively greater amounts of dense glandular tissue remaining in the upper outer quadrant of the breast and darker fatty areas in the medial and lower part of the breast. In some women, only fatty tissue is left after the menopause (Fig. 2-4).

It is important to know about the relative decrease in breast tissue and breast density over time. Increases in breast density in normal women occur only in pregnant and lactating women, or in women starting exogenous hormone replacement therapy. Unexplained generalized increases in breast density may indicate breast edema or inflammatory cancer. New focal density should prompt investigation because a developing density may represent a cancer.

Breast tissue is usually symmetric, or “mirror image,” when comparing left to right mammograms, although 3% of women have normal asymmetric glandular tissue. Normal asymmetric glandular tissue is a larger volume of normal fibroglandular tissue in one breast than in the other, but with one breast not necessarily being larger than the other. One method of evaluating for symmetry is to view the left and right MLO mammograms back to back and the CC mammograms back to back. The glandular tissue pattern is usually fairly symmetric from side to side, and asymmetries are easily identified using this technique (Fig. 2-5A to C).

A normal mammogram does not usually change from year to year after taking into account the normal involution of glandular tissue over time. Because the mammogram stays the same from year to year, comparing old studies with current studies makes it easier to see new or developing changes. For this reason, older films of good quality are placed next to the new films to look for subtle change (see Fig 2-5D to H). Because subtle changes may take longer than a year to become evident, one should compare both last year’s films and films more than 2 years old (or the oldest films of comparable quality) to the new ones. If the mammograms are screen-film studies, the images are viewed on a high-intensity view box with the light parts of the films masked to block extraneous light. For full-field digital mammograms (FFDMs) viewed on soft copy, the images are displayed on high-resolution bright monitors in a dark room with little to no ambient light, comparing old mammograms to new ones in the display protocol.

Mammographic Findings of Breast Cancer

Mammographic detection of breast cancer depends on the sensitivity of the test, the experience of the radiologist, the morphologic appearance of the tumor, and the background on which it is displayed. Cause for a “missed” breast cancer can usually be traced to one of these factors (Table 2-1).

Table 2-1 Reasons for Missed Cancers

Errors in technique

Poor technique Poor positioning Cancer in location not included in standard field of view

Errors in detection Errors in interpretation Radiologist sees and perceives finding, incorrectly interprets finding as nonactionable Tumor morphology Tumor shape similar to background fibroglandular tissue displayed on the mammogram True negative study Tumor cannot be seen even in retrospect

Radiologists see breast cancers on screening mammography because they see pleomorphic calcifications or spiculations produced by the tumor. Radiologists also may see architectural distortion, asymmetric density, a developing density, a round mass, breast edema, lymphadenopathy, or a single dilated duct, which are the other mammographic signs of breast cancer. The radiologist has to not only see the finding, but to also recognize that the finding is abnormal and correctly interpret the study as needing further action (i.e., is “actionable”) (Box 2-5).

The mammographic signs of breast cancer listed in Table 2-2 are discussed in further detail in Chapter 3 on breast calcifications, Chapter 4 on breast masses, and Chapter 10 on clinical problems. The trick is to see the cancer, perceive it and have it register in one’s mind, then interpret the findings correctly and act on the finding.

Table 2-2 Mammographic Findings of Breast Cancer

Finding	Differential Diagnosis
Pleomorphic calcifications	Cancer (most common), benign disease, fat necrosis
Spiculated mass	Cancer, postsurgical scar, radial scar, fat necrosis
Round mass	Cyst, fibroadenoma, cancer, papilloma, metastasis
Architectural distortion	Postsurgical scarring, cancer
Developing density	Cancer, hormone effect, focal fibrosis
Asymmetry: focal or global	Normal asymmetric tissue (3%), cancer (suspicious: new, palpable, a mass containing suspicious calcifications or spiculation)
Breast edema	Unilateral: mastitis, postradiation therapy, inflammatory cancer Bilateral:systemic disease (liver disease, renal failure, congestive heart failure)
Lymphadenopathy	Unilateral: mastitis, cancer Bilateral: systemic disease (collagen vascular disease, lymphoma, leukemia, infection, adenocarcinoma of unknown primary)
Single dilated duct	Normal variant, papilloma, cancer
Mass with calcifications	Cancer, fibroadenoma, papilloma; exclude calcifying oil cyst
Nothing	10% of all cancers are false-negative on mammography

Between 10% and 15% of breast cancers are mammographically occult, which means that breast cancer is present but the mammogram is normal. Accordingly, if there are suspicious clinical symptoms or physical findings and the mammogram is negative, the decision for biopsy should be based on clinical grounds alone.

The ability of mammography to depict breast cancer is optimized by good mammographic technique and positioning, which produces the best chance to display suspicious findings against the normal breast background. Mammographic signs of breast cancer are not seen as well against a dense or fibroglandular background, which hides masses and tiny pleomorphic calcifications. Suspicious masses also may be lost in a “busy” background of round benign cysts or extensive benign calcifications that draw the radiologist’s attention away from the cancer. Therefore, the radiologist needs a systematic approach to the mammogram to ensure a consistent, reproducible search pattern. Later, a re-review of “danger zones” where cancers are commonly missed will help the radiologist avoid mistakes.

An Approach to the Mammogram

Many tools are available to help the radiologist correctly interpret mammograms (Table 2-3). The first is the breast history and physical findings. The breast history sheet alerts the radiologist to the patient’s risk factors for cancer and the patient’s pretest probability of cancer (see Fig. 2-1). The history sheet includes the patient’s clinical history of breast biopsies and a schematic diagram of their location so that old scars are not misinterpreted as cancer.

Table 2-3 Tools Used for Interpretation of Mammograms

Tool	Use
Breast history, risk factors	Evaluate patient’s complaint and risks
Technologist’s marks	Show skin lesions, scars, problem areas
Putting images back to back	Detection of asymmetry Look for whitest part of study

Bright light (SFM) View skin, dark parts of film Window/level (FFDM) Contrast for masses, calcifications Magnifying lens or magnifier Visualize mass borders, calcifications Old films Compare for changes CAD (if available) Look for CAD marks after initial interpretation

CAD, computer-aided detection; FFDM, full-field digital mammogram; SFM, screen-film mammogram.

A technologist or aide usually interviews the patient, marking the location of any palpable finding on a diagram on the history sheet. Positions of findings in the breast are described in breast quadrants, with the upper outer quadrant representing the breast quadrant nearest the axilla. Another way to describe a breast location is by using the “clock face” method, in which the location of breast findings is described as though a clock were superimposed on each breast as the woman faces the examiner (Fig. 2-6). This means that the upper outer quadrant in the right breast is between the 9- and 12-o’clock positions, but the upper outer quadrant in the left breast is between the 12- and 3-o’clock positions.

The radiologist then reviews the breast history sheet and the technologist’s marks (indicating masses, skin moles, biopsies, scars, or implants). The technologist may place special skin markers on moles or palpable masses before taking the mammogram to draw the radiologist’s attention for a specific purpose. The technologist should write down why the skin markers were placed to clarify their placement for the radiologist.

The radiologist then starts a targeted systematic review of each film (Table 2-4). The radiologist first evaluates the images for good positioning, contrast, and compression. Next, the radiologist looks at the dense breast tissue for symmetry between the left and right breasts, which should be symmetric. The radiologist then looks at the whitest, or densest, part of the mammogram to see whether there is a mass or distortion there.

Table 2-4 Systematic Approach to Interpretation of Mammograms

Search Pattern	Normal Findings
Overall Search
Evaluation of technique	Good technique
Fibroglandular symmetry	Breast tissue usually symmetric Asymmetric tissue in 3%; be alert for new, palpable, three-dimensional masses or suspicious calcifications
White areas in glandular tissue	No mass or distortion; white areas look like normal tissue on the orthogonal views
Targeted Search
Edge of glandular tissue	No “pulling in” or tent sign, no concave masses
Nipple/areolar complex	Nipple everted, no skin thickening
Retroareolar region	Normal ducts, vessels, nipple in profile on at least one view
Skin	2–3 mm in thickness, no edema
Axilla	Normal lymph nodes, normal variant axillary breast tissue
Retroglandular fat	All fat, no masses between glandular tissue and chest wall
Medial breast	Mostly fat, normal variant medial sternalis muscle
Film edge	No mass or spiculation from findings lying outside the field of view
Use magnifying lens or magnifier	No pleomorphic calcifications, subtle distortion, or masses
Use bright light (SFM) or adjust window/level (FFDM)	Evaluate dark areas as needed
Compare with old films	No change; be alert for a developing density, new or changing calcifications or masses
CAD	Do a second look of the marked areas; CAD comes last because it does not pick up all cancers

CAD, computer-aided detection; FFDM, full-field digital mammogram; SFM, screen-film mammogram.

The radiologist inspects all edges of the glandular tissue where it interfaces with fat. Abnormal findings along the glandular tissue edge include a “pulling in” or tethering of tissue (the tent sign) or masses that pop out along the glandular tissue edge. The radiologist looks at the skin/nipple/areolar complex for thickening or retraction. Next, the radiologist makes sure that the retroareolar region, the axilla, retroglandular fat, breast tissue at the film edge, and the skin are normal. The radiologist then searches for calcifications by using a magnifying lens (on screen-film mammograms) or an electronic magnifier (digital mammograms). The radiologist then compares the new films with older films of the same quality to evaluate for changes. If computer-aided detection (CAD) devices are used, that is done so only after the initial review of the mammogram. Computer-provided marks should function as a “second look,” because CAD misses some breast cancers that are only detected by the radiologist. In a prospective study of CAD on more than 9000 mammograms in an academic center, CAD and the radiologist found 13 of 19 cancers, CAD found 2 cancers undetected by the radiologist, but the radiologist found 4 cancers not marked by CAD. Because CAD does not find all the cancers, it should not be used alone to read mammograms. The radiologist should read the mammogram and then use CAD as a “second look”; in addition, if the radiologist sees a suspicious finding, he or she should work up that finding no matter what CAD says because CAD misses some cancers that the radiologist sees.

The following section details the individual components of the systematic approach to the mammogram (see Table 2-4). The first step is to look at the mammographic technique for good quality and then to look for symmetry between the breasts, which are usually symmetric. Sometimes breast tissue is asymmetric, meaning that there is more normal glandular tissue in one breast than the other; this is a normal variant, like having one foot bigger than the other. Normal asymmetry consists of a normal asymmetric volume of breast tissue, more in one side than the other. On the CC and MLO views, the glandular asymmetry should “spread out” and not look like a mass (Fig. 2-7). Normal asymmetry can also be caused by removal of fibroglandular tissue from one breast by biopsy, making the other breast look like it has more tissue. Normal asymmetries should have no suspicious calcifications, spiculations, or palpable masses. Normal asymmetries are stable when compared with older studies. They are composed of fibroglandular tissue. If the asymmetry is palpable, has suspicious calcifications or spiculations, is new, or is a mass, the asymmetry may represent cancer and should prompt a workup or biopsy.

The next step is to look at the white parts of the mammograms for masses. Radiologists see masses because they are whiter than the surrounding tissue. Alternatively, a round or spiculated mass edge is seen against fat. If a possible mass is present on one projection, the radiologist looks for the mass on the orthogonal view. To do this the radiologist measures the distance from the nipple to the mass and searches the orthogonal view for the mass at this distance (Fig. 2-8A). If the finding is seen on two views, it is considered a mass. If it is seen on only one view, it is called a density and represents either a summation shadow (see Fig. 2-8B and C) or a mass (see Fig. 2-8D to H) that is obscured on the second view. The decision to recall this type of finding and prompt a workup is based on the radiologist’s experience and the degree of suspicion of the one-view finding.

The radiologist next looks at all the normal glandular tissue edges where they interface with fat. A layer of fat typically surrounds the cone of normal fibroglandular tissue and should contain no masses. As part of the systematic review, the radiologist checks the fat all around the glandular tissue to make sure that no masses are present. These edges should be gently curving, scalloped, and without tethering. Masses at the glandular edge or in breast tissue can “pull in” the fat, producing a tent sign caused by productive fibrosis from cancer retracting the Cooper ligaments and breast ducts. In other cases, tumor spiculation produces straight lines extending into the glandular tissue that draw attention to a mass at the center of the radius of spicules (see Fig. 2-8F). Subtle equal-density cancers can be difficult to detect, but looking for secondary signs of straightened lines in glandular tissue or tethering of the glandular tissue edge guides the radiologist to the cancer.

The radiologist then sees if the nipple is everted and reviews the complex structures of ducts and vessels in the retroareolar region. The nipple should be seen in profile on at least one mammographic view. If the nipple is not in profile on at least one view, the nipple may overlie the retroareolar region and obscure a mass, or it might be retracted by cancer. If the nipple is not seen in profile on any view, the mammogram should be repeated with the nipple in profile. If the nipple is truly inverted on the mammogram, the radiologist should check the breast history form to see if it was inverted at birth (normal variant) or if the nipple inversion is new. New nipple inversion is of concern for a retroareolar cancer and prompts a workup.

Normal breast skin is approximately 2 to 3 mm thick on the mammogram, and normal subcutaneous fat is dark. The skin should be smooth all around the breast and not pulled in (Fig. 2-9). Skin thickening greater than 2 to 3 mm that is asymmetric to the contralateral side is abnormal and is especially worrisome if the subcutaneous tissue has become gray and the thin tethering lymphatics and ligaments become thick and trabeculated. This is worrisome for breast edema. In general, skin thickening from cancer should be investigated.

The axilla normally contains lymph nodes, which are smooth oval or kidney bean-shaped masses containing fatty hila on the mammogram (Fig. 2-10A). Lymph nodes that grow larger become dense, round, and lose their fatty hila; they represent lymphadenopathy and are abnormal (see Fig. 2-10B).

Axillary breast tissue is a normal variant and consists of breast tissue in the axilla. Axillary breast tissue develops along the normal nipple line that extends (in animals) from the axilla along the chest to the abdomen. Axillary breast tissue can be, but is rarely, attached to an extra nipple. Noncompressed axillary breast tissue can simulate a mass, but it can be separated into its normal fibroglandular components by spot compression (see Fig. 2-10C and D). Spiculated masses in the axilla can mimic normal lymph nodes or axillary breast tissue. Any masses in the axilla should be scrutinized carefully to make sure they are normal lymph nodes or axillary tissue and not cancer (see Fig. 2-10E to G).

A few locations in the breast usually contain fat and deserve both special mention and a second look. The first is the medial portion of the breast, which usually becomes fattier over time. Masses or densities in the medial part of the breast are in a “danger zone” and should be scrutinized carefully because usually only fat is present here. The only exception is the normal sternalis muscle seen on the CC view near the chest wall. A second “danger zone” is the retroglandular fat, or fat between the cone of normal fibroglandular tissue and the chest wall. The area between the glandular tissue and pectoralis muscle should include only fat, with the only exception again being the sternalis muscle. This retroglandular fat is what Dr. Laszlo Tabar called “no man’s land.” Any masses here are abnormal and should be worked up. The third “danger zone” is the film edge at the chest wall. Here, the hint of a mass edge or spiculations may barely stick out into the field of view and suggest that a tumor is not fully imaged on the mammogram. In these cases, only special mammographic views will display the mass.

The radiologist last looks for pleomorphic calcifications with a magnifying lens (for screen-film studies) or an electronic magnifier (for FFDMs). Radiologists should look at screen-film mammograms with the magnifying lens until they see dust, which ensures that they have looked hard enough to find the calcifications that form in breast cancer. For screen-film mammography, the radiologist uses a hot light to illuminate dark portions of the mammogram as needed. For FFDMs, the images are viewed at optimal windowing and leveling to see calcifications, and the radiologist views all portions of the images under electronic magnification that shows skin pores to make sure the films are displayed at a high enough magnification to display tiny calcifications in cancer.

The radiologist then compares the current mammogram with older films of the same quality to check for developing densities and to look for new or progressive changes.

The radiologist last uses CAD (if available) and does a “second look” of findings marked on the mammograms by the CAD system.

By law (Mammography Quality Standards Act [MQSA]; P.L. 102-539), all mammograms must have a summary BI-RADS® code that indicates the radiologist’s final impression of the study. Both the BI-RADS® number and the words must be spelled out in the report (Box 2-6). Yearly, federal inspectors read mammographic reports at all U.S. facilities and check them for BI-RADS® summary codes and words. It is against U.S. federal law to exclude the BI-RADS® codes and words on mammogram repeats. Both monetary fines and jail sentences can be imposed on facilities that do not comply with MQSA.

The first BI-RADS® category, category 0, is used for screening recalls or when more studies are needed at the end of a case to make a final assessment. Categories 1 and 2 are used for normal mammograms or for findings requiring no action. Category 3 is used for findings thought to have less than 2% chance of malignancy and for which a short-term, 6-month follow-up mammogram may be implemented, with the expectation that the finding will be stable. Specifically, this category is often used for smooth noncalcified benign-appearing masses, benign-appearing clustered punctate calcifications, or benign-appearing focal densities in appropriate clinical settings. Category 4 encompasses a wide variety of findings for which biopsy is recommended. Category 4 can be further subcategorized into 4A, 4B, and 4C for lesions that require biopsy but with a low, intermediate, or moderate suspicion for cancer, respectively. Category 5 is reserved for mammographic findings highly suggestive of cancer, with a greater than 95% likelihood of cancer. Category 6 is intended for cancers for which a known diagnosis has been established before definite therapy such as surgery or chemotherapy. For example, women with large breast cancers diagnosed by percutaneous core biopsy who will be undergoing subsequent neoadjuvant chemotherapy would be designated category 6.

Diagnostic Versus Screening Mammography

There is a crucial difference between screening and diagnostic mammography. Diagnostic mammography is used for symptomatic women or for women with findings detected on screening mammography (Table 2-5). A radiologist is on-site for diagnostic mammograms to personally guide the workup by using special mammographic views or ultrasound.

Table 2-5 Screening versus Diagnostic Studies

Screening

Asymptomatic women CC and MLO mammograms Films taken and patient released

Diagnostic

CC, craniocaudal; MLO, mediolateral oblique.

Screening mammography is performed without a radiologist on-site. Screening mammography is meant for asymptomatic women. The usual scenario for a screening mammogram is that an asymptomatic woman has her mammogram and goes home. A radiologist reads the mammogram later. In the United States, screening includes two views of each breast—CC and MLO projections of the left and right breasts.

Women with lumps or symptoms need diagnostic mammograms, not screening mammograms. From 10% to 15% of all cancers are not seen at screening mammography; this usually happens in women with palpable breast lumps that are the cancer. Screening studies can result in false-negative findings even when the woman has felt her own lump. The false-negative screening mammogram may delay diagnosis. Some cancers that are felt as a lump may need tangential views, spot views, or ultrasound to reveal their presence. The extra studies are only done with a diagnostic mammogram, in which the radiologist recognizes the danger of the palpable mass and gets the other views on ultrasound. Therefore, women with lumps or symptoms need to undergo a diagnostic rather than a screening mammogram because the on-site radiologist can recognize the woman’s problem and target a dedicated workup to that problem to find the cancer.

Additional Views to Confirm or Exclude the Presence of a True Lesion

Radiologists use additional mammographic views in three common scenarios: to confirm or exclude a real lesion, to localize or triangulate a true lesion, and to characterize a true lesion (Box 2-7). A common reason to use additional views is in the setting of a “one-view-only” finding. Specifically, the radiologist sees a finding on one view that is not reinforced on the orthogonal view. Additional special views determine whether the finding is real. The first step is to estimate the finding’s location on the orthogonal view by measuring the distance from the nipple to the finding. The breast tissue is scrutinized along a radius of the same distance on the orthogonal view to identify the finding (see Fig. 2-8A). If the finding shows up on the second view, it is considered a true finding and the radiologist then uses additional views to characterize the lesion. If the finding is invisible on the second view, it may represent a true finding hidden on the second view or a fortuitous summation of normal breast tissue.

Many fine-detail mammographic views can be used to determine whether a “one-view” finding is a true lesion or a summation shadow (Box 2-8 and Tables 2-6 and 2-7).

Table 2-6 Mammographic Views Used to Visualize and Characterize Findings

Mammographic Problem	Mammographic View
True finding versus summation	Rolled views, spot view, step oblique views; repeat the same view
Triangulation	Line up CC, MLO, and ML views and draw an imaginary line through the lesion Use rolled views to determine whether the mass is upper or lower

Outer breast finding XCCL, Cleopatra Inner breast finding XCCM, cleavage view, spot view Upper breast finding Compression from below (or caudal-cranial view), upper-breast-only view Retroareolar finding Spot compression with the nipple in profile Lower inner finding Superior-inferior oblique Palpable finding Spot compression over the mass or a tangential view Characterization of a mass Magnification, spot magnification, or calcification views

CC, craniocaudal; ML, mediolateral; MLO, mediolateral oblique; XCCL, laterally exaggerated craniocaudal; XCCM, medially exaggerated craniocaudal.

Table 2-7 Mammographic Views and Abbreviations Used to Describe Them

View	Abbreviation
Craniocaudal	CC
Mediolateral oblique	MLO
Mediolateral	ML
Lateral-medial	LM
Laterally exaggerated craniocaudal	XCCL
Medially exaggerated craniocaudal	XCCM
Cleavage view	CV
Rolled view laterally	RL
Rolled view medially	RM
From below	FB

By convention, the side (left or right) precedes the view abbreviation.

From Mammography quality control manual, Reston, VA, 1999, American College of Radiology.

A “one-view” finding often prompts requests for “rolled views.” Rolled CC views separate normal fibroglandular elements into their individual components (see Table 2-6). The technologist “rolls” the breast tissue so that the top of the breast is rolled toward the axilla and then recompresses the breast. The bottom of the breast is now directed toward the sternum (Fig. 2-11A). This action rolls the fibroglandular components that form the “fake mass” away from each other. On the rolled view a summation shadow is separated into its normal fibroglandular components and the mass goes away (see Fig. 2-11B to G). On the other hand, true masses retain their shape and size on the rolled view.

Another way to separate true masses from fake ones is to use spot compression. A small compression paddle is used to compress tightly and directly over a finding. This provides greater compression on the area of interest. If used to determine if a finding is a real mass or a superimposition, spot compression separates fake summation shadows into normal fibroglandular components. If the finding is a real mass, the mass should persist within the spot compression field of view (Figs. 2-12 and 2-13). A true mass will retain its shape, size, and density, whereas a summation shadow will disperse into its fibroglandular components. It is important to perform the spot view in the projection in which the finding is best seen or displayed against fat to increase the chance of discovering if it is real (Fig. 2-14).

Step oblique views are mammograms obtained at slightly different oblique angles (i.e., 60, 50, 45 degrees) that throw fibroglandular elements into slight variations of obliquity. As with rolled views, true lesions should persist on multiple-step oblique views. Summation shadows, on the other hand, will separate into their fibroglandular components.

In all cases in which a mass is suspected, ultrasound provides indispensible information. The negative ultrasound confirms findings on “negative” mammograms. If the ultrasound is positive, a mass is confirmed. A repeat mammogram with a marker over the ultrasound-detected mass may show ultrasound findings that correspond to the mammographic findings and show a mass. If they do not correspond, more workup is needed (see Fig. 2-14 G to K).

Triangulation

Triangulation is the process of localizing a finding within the breast on two orthogonal views. Triangulation provides a clear three-dimensional position of a finding for subsequent imaging or biopsy. Triangulation is commonly used when a finding is seen on only two of the three standard mammographic views (CC, mediolateral [ML], and lateral views). For example, a finding might be seen on both the lateral and MLO views, but not on the CC view, and one has to find the lesion before needle localization. Or there is a finding on CC and MLO screening, and the radiologist needs to see it on the lateral view to guide ultrasound.

To predict a finding’s location from the CC and ML screening views, place the CC and MLO views so that the breasts face the same direction and the nipple is at the same level. An imaginary line drawn through the lesion on the CC and MLO views will predict the lesion’s location on the ML view. If CC, MLO, and ML views are available, place the MLO between the CC and ML views, with the nipple at the same level on each view (Figs. 2-15 and 2-16). An imaginary line drawn through the lesion on any two of the three views in which it is seen will predict where it will be on the third view.

Sometimes suspicious findings are thought to be true findings but are seen only on the CC view and not on either the ML or MLO views. Rolled CC views can show if true masses are located in the upper or lower breast. One does this by comparing the rolled view with the standard CC view. The technologist does a “rolled laterally” view by rolling the top of the breast toward the axilla and the bottom of the breast medially. An upper breast mass should roll laterally with the rolled upper breast tissue. A lower breast mass should roll medially with the lower breast tissue. The radiologist looks at the “regular” CC view and sees how the finding moves on the “rolled laterally” view. If the mass moves toward the axilla, the mass must be in the upper portion of the breast. If the mass moves medially on the “rolled laterally,” the mass must be in the lower portion of the breast (Figs. 2-17 and 2-18).

Visualizing Findings in “Hard to See” Locations

The following section details standard mammographic projections modified to visualize findings in specific “hard to see” locations that are commonly missed by standard CC, MLO, and ML views. It is not uncommon to see a suspicious lesion on one view and not see it on the orthogonal projection. This can be because of the patient’s body configuration or because the location of the finding makes it hard to see on the mammogram.

Some lesions are located in the extreme outer part of the breast not included on the standard CC view. A view that sees more of the outer breast is the CC view exaggerated laterally (XCCL). The technologist obtains an XCCL by modifying a standard CC view. She rotates the patient’s body to display more outer breast tissue than is seen on a standard CC view and excludes the medial portion of the breast (Fig. 2-19). This projection sees more outer breast, but doesn’t see the inner breast (Fig. 2-20).

The Cleopatra view also includes more outer breast tissue. In this view, the patient rotates laterally, as in the XCCL, but also leans obliquely like Cleopatra reclining on a bed of pillows (see Fig. 2-20E). The Cleopatra view includes much more of the outer part of the breast while excluding inner breast tissue. But unlike the XCCL, which is taken with the patient standing straight up, the Cleopatra view is taken with the patient leaning slightly backward and oblique.

For inner breast lesions, CC views exaggerated medially (XCCM) image the medial portion of the breast while excluding the outer breast tissue (Fig. 2-21A and B). Another view that visualizes the inner breast is the cleavage view (CV), or valley view, which includes the medial portions of both breasts on the image receptor in a modified CC projection. Such views allow visualization of even more of the inner part of the breast than is seen on standard CC views, but also images some of the opposite inner breast (see Fig 2-21C to E).

Some lesions are so close to the chest wall that they are hard to image with normal-sized compression paddles. The small spot compression paddles can get closer to the chest wall. You can use the small spot compression paddles to image extremely inner or deep lesions because they are smaller than the bulky normal compression paddles.

Some lesions in the upper part of the breast are so far back against the chest wall that they can be pushed out of the field of view by the compression paddle (Fig. 2-22). This problem can be solved by the from-below (FB) or caudal-cranial view. For this view, the image receptor is placed on the upper part of the breast. The breast is then compressed from below, excluding the lower part of the breast but including tissue high on the chest wall. In another approach for imaging lesions high on the chest wall, the image receptor is placed on the midportion of the breast with the lower portion excluded; this approach, first described by Sickles and colleagues, incorporates more of the upper portion of the breast because the compression paddle does not have to include lower breast tissue in the field of view.

Another area that is hard to see is the region immediately behind the nipple, which can be hidden by adjacent blood vessels and ducts. Spot compression compresses normal ducts, blood vessels, and tissue while pulling the nipple into profile (Fig. 2-23A and B). The nipple should be in profile on at least one view to see the retroareolar region; otherwise, the nipple may hide a cancer.

Lesions in the lower inner part of the breast are very hard to see. A superior-inferior oblique (SIO), or reverse oblique, view visualizes the lower inner breast. In this view, the technologist places the imaging receptor on the medial part of the breast and the compression plate on the superior breast while the patient leans over the imaging receptor (Fig. 2-24A and B). The compression paddle approaches the breast from the superior axillary side, allowing more of the inner breast tissue to be visualized.

Palpable findings imaged near the periphery of the breast are seen better with spot compression. This type of spot compression tangential to the palpable finding can push the mass against subcutaneous fat, allowing it to be seen. Spot compression directly over the palpable mass, previously known as a lumpogram, also can show masses by compressing the surrounding glandular tissue away from the suspicious finding (Fig. 2-25).

Additional Views to Characterize True Findings

After the radiologist determines that a mass or cluster of calcifications is a true finding and triangulates its position within the breast, additional mammographic views are used to characterize the finding (Box 2-9). Microfocal spot air-gap magnification views of clustered calcifications sharpen and separate calcification forms and display calcifications not detected on nonmagnified studies. Magnification can also depict mass shapes and margins to greater advantage, showing spiculated or irregular margins not discernible at lower resolutions (Fig. 2-26). Spot compression magnification views not only provide greater visualization of the region of interest by pushing fibroglandular tissue away from the finding, but also produce higher resolution of mass margins and calcification shapes. Thus, spot compression magnification mammograms are a mainstay of the radiologist’s diagnostic tools to characterize both masses and calcifications.

Summary

This chapter summarizes breast cancer risk factors, describes the signs and symptoms of breast cancer, and outlines a systematic approach to the mammogram to avoid diagnostic mistakes. A standardized, reproducible approach to the mammogram and re-review of mammographic “danger zones” in which cancers are commonly missed helps radiologists to avoid mistakes. After the radiologist discovers a finding, the radiologist has three duties: to determine whether the finding is real, to specify its location within the breast, and to characterize the finding to make a diagnosis. Modifications of standard views and fine-detail mammograms help the radiologist make these determinations.

Key Elements