Errors and mistakes in breast ultrasound diagnostics.

Sonomammography is often the first additional examination performed in the diagnostics of breast diseases. The development of ultrasound imaging techniques, particularly the introduction of high frequency transducers, matrix transducers, harmonic imaging and finally, elastography, influenced the improvement of breast disease diagnostics. Nevertheless, as in each imaging method, there are errors and mistakes resulting from the technical limitations of the method, breast anatomy (fibrous remodeling), insufficient sensitivity and, in particular, specificity. Errors in breast ultrasound diagnostics can be divided into impossible to be avoided and potentially possible to be reduced. In this article the most frequently made errors in ultrasound have been presented, including the ones caused by the presence of artifacts resulting from volumetric averaging in the near and far field, artifacts in cysts or in dilated lactiferous ducts (reverberations, comet tail artifacts, lateral beam artifacts), improper setting of general enhancement or time gain curve or range. Errors dependent on the examiner, resulting in the wrong BIRADS-usg classification, are divided into negative and positive errors. The sources of these errors have been listed. The methods of minimization of the number of errors made have been discussed, including the ones related to the appropriate examination technique, taking into account data from case history and the use of the greatest possible number of additional options such as: harmonic imaging, color and power Doppler and elastography. In the article examples of errors resulting from the technical conditions of the method have been presented, and those dependent on the examiner which are related to the great diversity and variation of ultrasound images of pathological breast lesions.

Dynamic development of ultrasound imaging techniques (US), particularly the introduction of Doppler ultrasound, harmonic imaging, extended field of view, compound imaging and elastography, enables more and more precise visualization of focal lesions in breasts and the differentiation of their character( (figs. 1, 2). Nevertheless, ultrasound is not a method deprived of limitations, which result inter alia from the technical conditions of the method and also from the great diversity and variation of ultrasound images of normal breasts and pathological lesions which depend on:

Fig. 1

Breast cyst. A. Basic examination. B. The same cyst after the use of harmonic option. Lack of reverberation, cyst borders clear

Fig. 2

Breast cancer – basic examination. A. Focal lesion in breast with blurred borders (arrows). B. After the use of harmonic option the lesion has typical ultrasound features as in malignant lesion pattern (arrows)

the age of a patient;

their hormonal condition, including menstrual cycle phase, lactation, postmenopausal period, the use of contraception or hormone replacement therapy (HRT);

breast surgeries undergone, inflammations, traumas, biopsies (particularly core biopsies and vacuum-assisted mammotomic biopsy) or radiotherapy.

The presence of so many factors affecting morphological breast image means that there is no strictly specified pattern of the normal US breast image to which one could relate pathological lesions diagnosed in US examination(.

Errors made in breast ultrasound diagnostics usually result from many factors, beginning from an inappropriate quality of the ultrasound machine and its settings, through insufficient knowledge and experience of the examiner, to the character of some breast diseases not having their unequivocal image in US examination.

Errors dependent on technical aspects

Among technical errors which might cause misinterpretation of the US image of the examined focal lesion one can number inter alia artifacts resulting from the volumetric averaging in near and far field. An artifact in the near field can result in lesions localized at depths up to 10 mm not being visualized and small hypoechogenic cancers with hyperechogenic halo may be presented as hypoechogenic lesions. In order to eliminate this type of artifact, use a standoff pad or thick layer of gel is recommended. With particularly large breasts volumetric averaging artifacts in the far field result from the averaging of cyst echogenicity with normal tissues echogenicity localized at the same depth. As a result we obtain a complex cyst or solid lesion image without circumscribed margin (fig. 3).

Fig. 3

Complex cyst (arrow) of uncircumscribed margin, with acoustic shadow behind the lesion, insusceptible to compression, mimicking solid lesion – BIRADS-usg 4

Inappropriate setting of general enhancement or time gain curve (TGC) can have an influence on incorrect differentiation of focal lesions, e.g. neoplastic lesions and cysts. They should be set so that fat tissue echogenicity is identical in preglandular, glandular and post-glandular zone. Otherwise fat tissue echogenicity differences at different depths can lead to an incorrect assessment of focal lesion echogenicity, which is assessed in relations to fat tissue( (fig. 4).

Fig. 4

Hyperechogenic focal lesion in relation to fat tissue, of identical echogenicity in particular zones

The appropriate range of the ultrasound beam should include the chest wall. To improve penetration, an increase in general beam enhancement and/or compression force on the examined breast can be used. In the case of large breasts, breasts during lactation, breast inflammation, inflammatory cancer or breasts with radiation lesions, the number of errors can be decreased using a linear transducer of lower frequency, e.g. 5 MHz.

The last group of technical artifacts are artifacts present in cysts or dilated lactiferous ducts; they include reverberations, comet tail artifacts and lateral beam artifacts (fig. 5). In these situations transducer head rotation or its slope, the use of harmonic imaging or real time compound imaging may be useful(.

Fig. 5

Simple cyst – BIRADS-usg 2, lateral beam artifacts (arrows)

Examiner dependent errors

These can be divided into:

false negative results – where the assessed lesion is incorrectly identified as too low category in BIRADS-usg classification relative to the histologic verification;

false positive results – where the assessed lesion is identified as to too high category in BIRADS-usg classification relative to the histologic verification.

This can result from:

the similarity of some benign lesions and normal breast structures to malignant neoplastic lesions (false positive results);

the similarity of some malignant lesions to normal breast structures or benign lesions (false negative results);

the characteristics of some breast diseases, with the absence of focal lesion (both false negative and false positive results);

lack of visualization of the lesion by the examiner (false negative results);

technical aspects (false positive and false negative results).

False negative results

The example can be focal lesions of malignant carcinomas which can mimic normal breast structures or benign lesions, e.g. ductal carcinoma in situ, invasive ductal carcinoma of high grade of histopathological malignancy, mucinous carcinomas, medullary carcinomas, metastases to breasts and also carcinomas in cysts and papillary carcinomas(. Papillary neoplastic lesions may mimic benign papillomas and other benign hyperplasias (in the assessment of their character and in identifying their BIRADS category one should take into account their size, localization and ultrasound structure) (fig. 6)(.

Fig. 6

Ductal carcinoma in situ (DCIS) presenting itself in the US examination as dilated lactiferous duct with dense contents, insusceptible to compression, circumscribed margin of the walls – BIRADS-usg 3

In order to avoid incorrect diagnoses, one should use as many techniques enabling lesion character differentiation as possible, such as harmonic imaging, vascularization pattern assessment, compressivity in conventional imaging and in sonoelastography. This last method is particularly useful in the differentiation of focal lesions (including invasive carcinomas) from fat lobules which undergoes greater deformability in comparison with solid lesions(. Fat lobules may be incorrectly interpreted as solid lesions BIRADS 3 or BIRADS 4 or some malignant neoplastic lesions if they have decreased echogenicity or have uncircumscribed margins in US examination.

False positive results

Identifying benign lesions and normal structures incorrectly as malignant neoplasms results most often from alack of knowledge of anatomy and the changes related to the regression of the lobules and stromal fibers of breasts resulting from aging (that is the ratio of glandular and fat tissue in the breast). In the US image hypoechogenic areas mimicking focal lesions are visible, which are in fact fat tissue (fig. 7). In such situations a series of sections should be done in order to confirm or eliminate the connection of the “lesion” with the surrounding fat tissue. Most often fat lobules are wrongly unainterpreted as fibroadenomas. Conversely, complex fibroadenomas, sclerosing, giving acoustic shadow or having angular edges are often classified to BIRADS 4 category, although in the majority of cases they are benign (fig. 8)(. At the present stage of technological ultrasound development it is not possible to differentiate between them in the US examination. Similarly, it is impossible to distinguish between papillary neoplasm hyperplasias in the cyst lumen and papillary metaplasia. Doppler assessment of lesion vascularization helps to identify BIRADS category (4 or 5), in which carcinomas and intercystic papillomas usually have a vascular stem (fig. 9). However, the most important factor is the histopathological verification of the lesion(.

Fig. 7

A. Hypoechogenic focal lesion in breast glandular tissue (arrow). B. The same lesion in a different section has the connection with surrounding fat tissue (arrows)

Fig. 8

Solid, hypoechogenic lesion, oval, of uncircumscribed margin, blue in elastogramme (as in lesion insusceptible to deformation). BIRADS-usg 4, Tsukuba 4. In histopathological examination: fibroadenoma with sclerosing

Fig. 9

Hyperechogenic solid lesion localized intraductally, with visible vascular stem, insusceptible to compression, in patient with high risk nipple discharge. BIRADS-usg 4. In histopathological examination: papilloma

In this group of false positive diagnoses there are also architecture disorders and lesions giving acoustic shadows such as fat tissue necrosis, adenosis sclerosans, scars after surgical procedures, biopsies, radial scar or focal fibrosis (fig. 10).

Fig. 10

Hypoechogenic glandular tissue architecture distortion of spicular margins, with acoustic shadow (arrow). BIRADSusg 5. In histopathological examination: focal fibrosis

Fat tissue necrosis demands special attention; depending on the reason and duration it may look like a simple cyst, complex cyst or solid lump. In later stages of the disease there are angular edges giving an acoustic shadow which resembles the US image of a cancer with desmoplastic reaction. In order to differentiate, one should asses the vascularization of the lesion – fat tissue will not exhibit the features of the flow presence, it will undergo compression and in elastogrammes it will show the soft lesion pattern (fig. 11). In the case of postoperative scars or after biopsies, the differentiating element is the medical history. In cases of negative history, these lesions are classified as BIRADS-usg 4 or 5 and demand histopathological verification.

Fig. 11

A. Hypoechogenic oval lesion of the dimension of 6×4 mm, BIRADS 3. B. In elastogramme homogenous lesion, of blue color (deformation susceptible lesion pattern), of the average value E = 13 kPa. In cytological examination fat tissue

The last group of cases, both false negative and false positive, are lesions which do not form an image of a focal lesion. Among this group of false negative lesions one can number malignant neoplasms such as carcinomas in situ of low grade of histopathological malignancy, lobular carcinomas, early stages of other carcinomas, in particular of small size(. In the case of lobular carcinomas, in which neoplastic cells bands are scattered among normal stromal cells in the US examinations, they are often visible as acoustic shadows among echogenic fibrous tissue (fig. 12). These images are highly unspecific and may occur in benign and malignant hyperplasia. Because in such cases mammography examination (MMG) has a limited sensitivity, histopathological verification should be performed(. False positive lesions which do not form focal changes also include fibrocystic dysplasia, post-traumatic, postoperative, post-radiation lesions or fat tissue necrosis.

Fig. 12

Solid hypoechogenic lesion with prevalence of superiorinferior dimension over latero-lateral dimension, giving acoustic shadow, in color Doppler with pathological vessels, with hyperechogenic “halo”, BIRADS-usg 5. In histopathological examination: lobular invasive cancer

General rules of breast US examination which enable the minimization of the number of diagnostic errors

Before the US examination, the doctor should perform a medical history and physical breast examination, he should also refer to previous imaging examinations performed (fig. 13).

Fig. 13

Classical US image as for a malignant lesion in the breast of 50 years old woman who had mammography performed in which no potentially malignant lesions were stated. The breast with predominance of glandular tissue

A US examination performed according to the Polish Ultrasound Society breast examination standards (fig. 14)(.

Fig. 14

Segmentally dilated lobular lactiferous duct with tissue echoes (arrows). In FNAB neoplastic cells. In histopathological examination after surgical treatment – ductal carcinoma in situ

Treating each pathological focal lesion or lesion in lactiferous ducts visualized in US examination which does not fulfill the criteria of a benign lesion, as suspected of malignant character until the final histopathological diagnosis (fig. 15).

Fig. 15

Breast cyst with tissue echoes in its lumen (arrow). These echoes did not change their localization after the change of breast position during examination. Final diagnosis: papilloma in the cyst

Very careful analysis of the visualized focal lesions in breasts, both clinical (palpable) and subclinical (below 5 mm in diameter); small focal lesions in breasts usually do not have the typical morphology of a benign or a malignant lesion (fig. 16).

Fig. 16

The first US examination in 37 years old woman who experienced repeated breast soreness in consecutive menstrual cycles. Focal lesion in glandular tissue of the diameter of 6 mm (arrows). In FNAB neoplastic cells. In histopathological examination: glandular cancer

Obeying the rule that each focal change in breast in BIRADS-usg 4 and 5 category is confirmed by microscope examination (FNAB, CB) (fig. 17), whereas in BIRADS-usg 3 category it is possible to perform FNAB or refer the patient to a control examination in 6 months(.

Fig. 17

Pathological focal lesion in breast (arrows). In the US examination the pattern as for a benign lesion. Histopathological diagnosis: medullary breast cancer

Very careful ultrasound examination of breasts with cystic changes, particularly multiple, which can cover small foci of breast cancer (fig. 18). Referring for further diagnostics of all fluid-filled lesions in breasts which do not fulfill classical criteria of breast cysts (that is BIRADS-usg 2).

Fig. 18

Focal lesion in breast of the diameter of 5 mm (arrow) among cysts. In histopathological examination: invasive ductal breast cancer

Precise ultrasound examination in women who have reported in medical history or currently have bloody discharge from the nipple, with its cytological assessment (fig. 19).

Fig. 19

Intraductal breast papilloma (arrow). In medical history reported bleeding from the nipple 1 month prior the US examination

Very careful performance of breast ultrasound examination in women with a predominance of glandular tissue with normal result of mammographic examination. In such cases many small, solid focal lesions which might be breast cancer are not visualized in MMG (fig. 20)(.

Fig. 20

Small, 7 mm in diameter, invasive ductal cancer of breast (arrow) in 45 years old woman with volumetric predominance of glandular tissue, who in previously performed mammography did not have any lesion suspected of malignancy

Very careful performance of the ultrasound examination of glandular breasts with features of a significant degree of remodeling by stromal tissues. Images obtained often mimic malignant lesions (fig. 21). It is necessary to refer these women for further diagnostics – biopsy, mammography, magnetic resonance mammography and systematic 6 monthly control US examination.

Fig. 21

A. Glandular breast cancer (arrows). B. Area of increased remodeling of glandular tissue by stroma (arrows)

The use of a standoff pad or great amount of gel in breast focal lesions localized superficially in order to optimize the image (fig. 22).

Fig. 22

Breast skin fibroma (arrow), the examination was performed with a standoff pad. US image of breast skin is indicated by small arrows

Careful performance of the ultrasound examination in women after mastectomy because of breast cancer and after breast conserving therapy – one should remember that they have an increased risk of breast cancer morbidity in the second breast or a recurrence incidence (fig. 23).

Fig. 23

Breast cancer recurrence (arrow) in woman with breasts of glandular structure. The recurrence was diagnosed 8 months after quadrantectomy performed because of invasive ductal cancer

Careful performance of the examination in women after breast focal lesion excision. The scar after surgical procedure in US examination may be similar to focal malignant lesion (fig. 24).

Fig. 24

Scar in the breast (arrows) after fibroadenoma excision

A group particularly exposed to more frequent breast cancer incidence are women with familial breast cancer. From the moment of receiving this information they should be included in the program of prophylactic breast cancer examinations. In high and very high risk groups of breast cancer morbidity one should perform alternate MMG examination and magnetic resonance examination every 6 months complemented by the US examination of breasts every 12 months(.

In all doubtful and diagnostically difficult cases one should consult other doctors in more specialized centers.

The diagnoses should be systematically verified and one's diagnostic mistakes should be analyzed.