Introduction
Malignant tumours (cancers) and benign diseases are very common in the breast. Aside from clinical history (disorders in the family, previous breast diseases/surgery, hormone therapy, personal well-being and complaints), inspection (external viewing) and palpation, which compose the so-called clinical breast examination, imaging procedures and especially mammography are of crucial importance in the detection and diagnosis of breast cancer and also other breast diseases. Mammography is a specialised radiography of the breast using x-rays for generating images of the breast. Its purposes are first early detection of breast cancer before symptoms (screening mammography) and second diagnosis in patients with symptoms such as a palpable lump (diagnostic mammography, also named clinical mammography).
This article—specifically aimed at summarising the most important information to be offered to women about mammography—updates a previous article published in 2012 [
1] by the European Society of Breast Imaging (EUSOBI), taking in consideration the most recent evidence in favour of mammography and of two mammographic technique tools now available for clinical practice: digital breast tomosynthesis (or simply
tomosynthesis) and
contrast-enhanced spectral mammography (CESM). Here we also took into account the recent position paper on screening for breast cancer by EUSOBI and 30 national breast radiology bodies [
2], which should be considered complementary to the current article.
Screening and diagnostic mammography
Mammography is the most important imaging procedure for breast cancer detection and diagnosis. The general aim is to enable early treatment of breast cancer, to improve survival rates and to reduce the need for aggressive treatment such as mastectomy [
3,
4], also in the current era of modern therapies [
5,
6]. It can be performed in a screening setting or a diagnostic setting. In both settings, whenever possible,
preference should be given to full-field digital mammography (not phosphor-plate computer radiography) instead of film-screen mammography, taking in consideration a number of relevant advantages for the women who get a mammogram and for the general population, including lower x-ray dose, higher image quality, possibility of post-processing, digital archiving, image transmission and no chemical pollution [
2,
7].
Scheduling/precautions
The best time for a less painful mammography to be carried out is from day 7 to day 12 after the beginning of the woman’s last menstruation. No particular scheduling is required after menopause, implying that for the majority of mammograms performed in the context of population-based screening programmes scheduling has no limitations. If the woman is pregnant, ultrasound is preferred as a first option.
Note B. You should bring images and reports from the previous mammograms (and from other recent breast imaging examinations) and give these to the radiographer or the radiologist before the procedure. This can be crucial for image interpretation due to the fact that some cancers are diagnosed only on the basis of changes that have occurred after a previous examination.
Technique/procedure
Mammography is performed using a dedicated x-ray unit. A particular radiographic technique is used requiring the compression of the breast for 5–10 s in order to deliver a low radiation dose and to obtain high-quality images. As already mentioned, it is standard practice to take two views per breast and additional views in special cases. The procedure is performed with the woman’s upper body undressed. All foreign objects (such as bras, necklaces, piercings, etc.) must be removed before the procedure. The woman will stand in an upright position in front of the machine. For each projection of each breast, the radiographer will place the breast on the plate and will carefully apply a progressive compression for 5–10 s. During breast squeezing, women may feel some pain or discomfort [
11].
It is important not to move during this short time. Immediately after acquiring the mammogram, the breast will be released from compression. The entire bilateral standard procedure, including preparation, takes approximately 5–10 min.
Note C. To reduce pain or discomfort due to breast compression and to get the best mammograms, you should relax during the procedure; in particular, the pectoral muscles should be relaxed. Follow the radiographer’s instructions exactly and bear in mind that heavier compression means a lower x-ray dose, higher image quality and easier diagnosis. If you previously experienced a painful mammography in the premenstrual phase, try to arrange the next one from day 7 to day 12 of your cycle.
After the procedure
When the procedure is over, the woman returns to the waiting room. In the case of screening mammography, she is usually only informed whether or not the acquired images are technically adequate. If no views need to be repeated, she may leave. She will receive a letter communicating that the mammogram is negative or she will be informed, usually through a phone call, that further assessment is needed (
recall). The first event is far more probable (over 90–95 % of cases). In some countries, only positive screening examinations (recalls) are communicated. In the case of diagnostic mammography, after checking the technical adequacy, the radiologist immediately informs the patient either that the examination is completely negative or that further assessment is needed, as already mentioned.
Note D. If you are recalled after a screening mammogram or you are asked to have an ultrasound after a diagnostic mammography, this does not mean that you have a cancer. The most probable result of this second examination, especially in the screening setting, is a higher level of certainty in stating that you do not have cancer! Less than 10 % of women recalled at screening are finally diagnosed with cancer. However, if a cancer were present, you would rightly like it to be diagnosed as early as possible.
Mammography report and classification systems
Diagnostic mammography and also diagnostic assessment of recalled women after mammography screening should be formally carried out by a certified breast radiologist. A detailed report should include a description of the clinical context, if relevant, as well as image findings, including breast density and structure according to different classification systems, interpretation of the described findings and a final conclusion with recommendations. In many European countries, standardised classification systems for the conclusions of mammography reports are used. A European system uses the five-level scale from R1 to R5, where R stands for radiography. R1 means no abnormalities, R2 benign findings, R3 equivocal findings, R4 suspected cancer and R5 strongly suspected cancer. A system developed in the USA, the Breast Imaging Reporting and Data System (BI-RADS) [
12], also used in many European countries, includes a similar scale, from BI-RADS 1 to BI-RADS 5. The main difference is for BI-RADS 3, which implies a very low probability of cancer (less than 2 %), allowing the possibility of waiting for a short interval (usually 3–6 months) before a repeat mammogram. Conversely, the R3 category indicates a probability of cancer that is higher than that of BI-RADS 3. Moreover, the BI-RADS score system also includes BIRADS 0 (examination insufficient for a diagnostic conclusion; further work-up needed) and BI-RADS 6 (evaluation of an already diagnosed cancer).
Note E. In practice, if you have an R4–R5 or a BI-RADS 4–5 finding, needle biopsy is recommended. In case of R3 or BI-RADS 3, meet your radiologist and ask for a detailed explanation of this result, of the risks and probabilities associated with different options.
No diagnostic test is perfect. This rule also applies to mammography. When thinking about screening, women should be aware that about 28 % of cancers can be missed [
13,
14], especially in pre-menopausal women and in those with dense breasts. This means that if we consider 1000 women getting a screening mammogram, if 8–10 cancers are present, 2 or 3 can be missed, mostly because they are difficult to distinguish from normal breast tissue. Still, mammography is the best proven method for screening average-risk women.
Note F. Do not underestimate the importance of breast symptoms (especially a new palpable lump, skin/nipple retraction or nipple discharge), regardless of the timing of your last negative mammogram. Go to your radiologist and ask for a visit. Tell her/him your symptoms and she/he will decide the best course of action for you. Conversely, not all suspicious findings visualised on a mammogram are cancers: depending on the level of suspicion, cancer is confirmed in a highly variable proportion of cases. When the suspicion is confirmed after further assessment, image-guided needle biopsy is mandatory before planning any treatment.
Note G. A suspicious mammographic finding is not a confirmed cancer. However, do not postpone further assessment and, if necessary, needle biopsy.
Radiation exposure from mammography
The radiation exposure for a mammogram is low. A study [
15] reported that undergoing repeated mammograms over a time period of 34 years (annual from age 40 to 55 years and biennial from 56 to 74 years) entails a risk of radiation-induced breast cancer equal to 1 in every 1000 women screened. The risk of breast cancer in the female population of western countries is equal to at least one in every ten women. The first risk is 100 times smaller than the second, while the reduction in breast cancer mortality thanks to early detection with screening mammography is about 40 % [
4]. Another study [
16], applying a mortality reduction rate of 43 % as an effect of screening mammography, also considering the “minimal” risk of radiation-induced cancers, found that biennial screening mammography performed in 100,000 women age 50–69 saves 350 lives. However, for the 40–49 age range, the problem of radiation effects depends on the estimated magnitude of radiation-induced BCs in this younger age interval and must be more carefully considered.
Importantly, even in the rare case of radiation-induced breast cancer, in a screening setting most of these will be detected early and treated. In symptomatic women, when a mammogram is necessary, the advantages always outweight the disadvanges, independently from the patient age.
Overdiagnosis
Not all the breast cancers diagnosed with screening are aggressive and fatal cancers. In the absence of screening mammography, some breast cancers—estimated to be about 6.5 %, with a range from 1 % to 10 % [
4]—would have remained totally free of symptoms because of the very slow growth of these types of lesions, which do not tend to advance outside the breast [
17]. However, these cancers cannot be distinguished from those that, if left undiagnosed and untreated, would be fatal. Thus, if we want to reduce breast cancer mortality, we must accept a rate of overdiagnosed cancers with the consequence of a rate of unnecessary treatment, mainly including surgery and radiation therapy. An effective representation of the balance between early diagnosis and overdiagnosis has been provided by the Euroscreen working group [
18]: for every 1,000 women screened from 50 to 69 years of age, 7–9 breast cancer deaths are avoided, 4 breast cancers are overdiagnosed, 170 women have at least one recall followed by noninvasive assessment with a negative result, and 30 women have at least one recall followed by invasive procedures with a negative result.
In practice, the probability of an individual woman’s life being saved is double that of being overdiagnosed.
New mammographic techniques: tomosynthesis and contrast-enhanced spectral mammography
Two further developments of digital mammography were recently introduced into clinical practice: tomosynthesis and CESM. Both techniques are intended to overcome some limitations of mammography by reducing summation effects (tomosynthesis) or by increasing contrast differences (CESM), especially, but not only, in women with dense breast tissue. In these women, tumours can be masked because of overlying breast tissue and lack of contrast to the adjacent normal breast tissue is common. So far, these techniques have mainly been proposed as an adjunct to mammography in women with inconclusive findings in their initial mammograms, with interesting results. Tomosynthesis has also been positively evaluated as a screening tool.
Frequently asked questions (FAQs)
How painful is breast compression for mammography?
Mammography is tolerated well by the vast majority of women. In particular, it is painless for about 40–50 % of women, a little painful for 40 %, rather painful for 12 % and very painful only for 4 %. Pain disappears immediately after the procedure for 76 % of the women, while it lasts several minutes for 13 %, several hours for 7 % and more than 1 day for 4 % [
11]. However, the advantages of compression are clear, and unnecessary pain may sometimes be avoided by suitable scheduling (see Note C). The radiographer will guide you through all the steps of the examination and will take care of minimising the discomfort during breast compression.
When should the first mammogram be done? What are the time intervals for further examinations?
Different recommendations are issued by different radiological and cancer societies as well by health authorities and governmental bodies. There is a general agreement on the usefulness of screening mammography from 50 to 70 years of age, with a time interval depending on several factors described above. Extension from about 40–45 to about 75 is now adopted by several screening programmes. When starting at 40, a 1-year interval can be recommended up to 45–50, considering the probable higher density and the possible faster growth of the tumour. After 50, the optimal interval may be decided based on personal history and breast density. If you have symptoms, mammography may be necessary for you at any age. If you are a woman with an increased risk for breast cancer (gene mutation carrier, multiple breast/ovarian cancer in the family), screening should start before age 40, according to your personal calculated risk level, access to special screening programmes, and other factors.
Note K. If you are invited to attend an organised screening programme, follow the programme’s planned interval. If you have any doubts about this time interval, or the usefulness of ultrasound as a supplemental screening method, consult your radiologist. If there are a high number of incidences of breast cancer in your family, especially at a young age and before menopause, you may need to have a screening with MRI [
9,
10]: consult your radiologist and/or a specialised centre (e.g. a family cancer clinic). Information on indications to MRI are available in a EUSOBI dedicated paper [
10].
What about screening mammography for women over 75?
The continuous increase in life expectancy prevents defining a clear cut upper age limit for screening mammography. A general suggestion is to continue screening with mammography for elderly women as long as their health is not significantly compromised by illness that drastically reduces life expectancy [
41,
42]. Discuss this decision with your radiologist.
Can women with breast implants or breast reconstruction undergo mammography?
Yes, in the majority of cases they can. Special views with back placement of the implant are commonly needed, as well as specific technical expertise by the radiographer. Exceptions where mammography cannot be performed are breast reconstructions after complete gland tissue removal. Mammography limitations due to the presence of implants can be counteracted by an accurate clinical breast examination and breast ultrasound.
Note L. Always tell the radiologist and/or the radiographer if you have breast implants.
Is x-ray radiation from mammography dangerous?
The x-ray radiation associated with a mammogram is low. See in this article the section “Radiation exposure from mammography” for a comparison between the risk of radiation-induced breast cancer and the reduction of breast cancer mortality due to mammography.
What is the role of new technologies like tomosynthesis and CESM?
The role of these new technologies is to help in the detection and diagnosis of breast cancers. Tomosynthesis is commonly accepted as an effective tool for evaluation of symptomatic patients and suspicious findings at screening mammography. Large studies in the screening setting showed that tomosynthesis allows the identification of more cancers than mammography and potentially reduces the number of women recalled for benign findings. So far, CESM has been evaluated in a limited number of small studies. It provides useful information of suspicious lesions, increasing the visibility of malignant lesions, in particular in women with dense breasts, and can be an alternative to contrast-enhanced MRI, especially in the case of contraindications to MRI or to gadolinium-based contrast injection as well as of difficult MRI availability.
Acknowledgments
The authors thank Europa Donna-The European Breast Cancer Coalition for reviewing the text to ensure that it can be easily understood by women who desire information about mammography.
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