Breast elastography has become a key complementary technique. A modality in the framework of breast pathology, complementary of B-mode imaging and colour doppler analysis. Breast ultrasound has provided morphological grayscale images and functional flow analysis of the soft breast tissues. Elastography now brings new physio-pathological information through the assessment of tissue elasticity. There are two different modalities: Real Time Elastography (RTE) and Shear Waves (SWE) ultrafast Imaging. Both techniques require a minimum adhesion to the skill rules for acquisition and interpretation so as to limit the operator dependant dimension and diagnostic errors. Elastography thus becomes perfectly reproducible with good accuracy in the different scores of the RTE or SWE classification. The aim of elastography in cancer screening is to achieve reliable lesion characterisation and better therapy monitoring/management.
- Strain Real Time Elastography (RTE)
- Shear wave Elastography (SWE)
- lesion identification
- Lymph node analysis
- prognostic + lesion aggressiveness
- oncologic management
No one denies anymore the use of ultrasound which is now part and parcel of the different techniques used in medical imagery for the diagnosis of mammary pathologies. The complementarity of these techniques (mammography, MR and ultrasound) is perfectly accepted, as each of them suffers from a certain number of shortcomings. The development of elastography has deeply improved the management of the monitoring of mammary lesions thanks to a better identification of the anomalies of the breast, a more accurate measuring of the lesions, a guiding of the biopsies of the lesions and of the lymph nodes, an approach to probably benign lesions, a management of those which are highly likely to be suspicious and a better planning of the surgical and therapeutic interventions. It is important to limit to the utmost the number of breast biopsies, when one bears in mind that between 40% and 50% of these biopsies concern benign lesions which, as a rule, do not require these punctures.
Echography (B-mode imagery-colour Doppler) can claim an excellent over 90% sensitivity, with a very good negative predictive value (NPV) (around 90%). But its specificity and its positive predictive value (PPV) are less accurate, by 40–60% according to various publications.
It is essential, when choosing an echography machine to select one with a good elastography attachment, as well as to have a minimum training to practice elastography so as to curb as much as possible the operator-dependent dimension of the examination, optimise the criteria of interpretation and finally ensure a good reproducibility of the results obtained.
It appears that the use of elastography has clearly contributed to limit the technical shortcomings of conventional echography. In order to achieve this, it is absolutely essential to abide by a minimum number of technical rules (like the correct positioning of the probe which must be horizontal and strictly perpendicular to the skin, as well as a good positioning of the patient in relation to the anatomical zones of the breast to be explored, and lastly a mastering of the micro-sismo-echography technique or vibrating technique or parkinson like vibrations (for Real Time Elastography Strain).
Though falling short of perfection, two important studies were commissioned in 2013 by EFSUMB (European Federation of the Societies of Ultrasound in Medicine and Biology):
2. Two elastography techniques
Two different sorts of medical equipment can make use of elastography:
Nuclear Magnetic Resonance (MR)
Ultrasound Echography (US). This latter technique is the only one currently used in daily practice;
US elastography is of two different types:
Real Time Elastography Strain (RTES) using an external constraint
Shear Wave Elastography (SWE) using an internal constraint.
For both techniques, the results of the ‘estimation of tissue stiffness’ are either qualitative or quantitative.
2.1 RTES: (SE)
This technique uses an external constraint induced to the tissue which is generated by the physician himself by positioning the probe in contact with the skin. The probe allows him to apply repetitive minimal compression/vibration to the breast tissue, the compression wave being propagated at the speed of 1500 m/s. The software of the echography machine allows the analysis of the relative movements of the different tissues thanks to the stress/strain ratio distribution providing an image of relative tissue stiffness, classified with the Tsukuba coloured criteria of stiffness of the lesion itself and of the surrounding tissues (classification in keeping with the BI-RADS radiological classification) with five scores :
Score 1—No difference between the different tissues
Scores 2 and 3: Increasing proportion of the stiffer zone
Score 4: typical permanent internal stiffness of the lesion itself
The real cut-off point between benign and malignant corresponds to the score 3–4 boundary.
The use of the (ROI) region of interest on the most reproducible frame (selected with cine-loop) can be placed to cover the lesion and its adjacent tissue (as softly as possible, ideally just under the skin) to allow calculation of the fat/lesion ratio.
These data increase the diagnostic confidence in the differentiation between benign and malignant diseases without adding significantly to the length of the examination.
The sensitivity is over 90%, the specificity 88% when adding US elastography in multicentric series of several thousands of breast lesions with a good accuracy and reproducibility .
A third dimension, that is a piece of histo-pathological information obtained through the assessment of time elasticity is achieved by the Shear Wave Elastography technique (SWE), the first two dimensions being morphological grey scale images on the one hand and functional flow imaging of soft tissue on the other.
The waves travel in these tissues at 1–10 m/s with Shear Waves.
Focused ultrasound beams are automatically generated at supersonic speed by the probe and received back for analysis. The analysis of the propagation of ultrasound wave trains in the tissue structures is the trademark of SWE.
A mind-boggling calculation capacity is needed to capture shear waves and measure their propagation speed at the frame rate of up to 20,000 images per second.
Shear waves propagate faster in hard tissue than in soft one. The shear wave speed can be converted in colour (optionally in grey scale) or in kilo Pascal (kPa).
A specific region of interest (ROI) of different stiffer parts of the lesion or of adjacent tissue gives precise information on the variations in stiffness. This measurement in kilo-Pascal is a characteristic of the SWE technique. It allows extremely precise results.
Fat elasticity varies from 3 to 9 kPa; glandular stroma elasticity from 11 to 50 kPa. The average figure for the elasticity of malignant lesions is higher than 100 kPa and can even reach over 150–200 kPa (in 13 published studies).
All the lesions with a figure higher than 50/60 kPa are to be biopsied, thanks to an impressive improvement in the sensitivity and the negative predictive value up to 100% according to EVANS. The specificity as well as the positive predictive value are also significantly improved with a better evaluation of the 3–4 BI-RADS cases which can thus be reclassified upward or downward as the case may be, which leads to a considerable reduction in the number of unnecessary biopsies (Figures 3 and 4) .
3. Limitations and artefact
Some cysts have heterogenous contents which are difficult to analyse.
The very superficial location of a lesion next to the skin, or on the contrary against a rib in a breast without fatty cover may cause difficulties by making it impossible to position the ROIs or achieve the fat to lesion ratios.
There exist ‘soft’ cancers of the cancer in situ type, colloid or mucoid cancers, diffuse ones (no mass cancers). On the other hand, mucinous cancers have been described by some as ‘hard’, between 95 and 270 kPa.
Lastly some old, very fibrous fibroadenomas may seem ‘hard’ but are without any hypervascularisation, and without very suspicious ultrasound signs. A perfect mastery of the technique of positioning the ‘elasticity boxes’ is essential for their correct analysis.
4. Contribution of elastography to the diagnosis of breast cancer
4.1 The coupling of conventional echography
The coupling of conventional echography (which underestimates the size of the lesions) with Strain or SWE elastography has resulted in a significant improvement in the measurement of the size and extent of the lesions (calculation of the longest axis, the perimeter and the extent). The histological sections and the SWE measurements were identical (give or take 2 mm) according to some authors. In its calculations, elastography integrates changes in extra cellular matrix, inflammation and stroma remodelling (myofibroblasts and collagen) in invasive cancers (Figure 12).
4.2 Echo-guided punctures
Echo-guided punctures are made easier in areas displaying maximum modification in elasticity. The centre of the tumour is not always the area with the highest density in cancerous cells (central necrosis) which are to be found in larger numbers at the periphery of the tumour (Figure 6).
Patients having a second reading echography after an MR showing subtle or difficult to interpret images have benefitted from a better biopsy carried out under echo-elastography (29% improvement of the sensitivity). Decrease in the number of false positives and 40–50% reduction of biopsies concerning benign lesions for which puncturing is not needed, thanks to an improvement in the sensitivity of mammary echography (Figure 7).
4.3 Better identification of the pathological lymph nodes
he analysis of the lymph nodes through echography and elastography requires a good deal of experience and a thorough exploration of all the zones of the breast where these nodes are to be found (axillary, para-sternal intra-mammary, intra-pectoral, supra-clavicular, mediastinal, contralateral axillary and internal mammary zones)
Most lymph nodes (75%) are to be found in the axillary zone.
90% of the lymph nodes larger than 5 mm can be identified .
The modifications of the lymph nodes can be inflammatory, related to a systemic disease, to granulomatosis, or lastly to a metastasis of melanoma, lymphoma or breast cancer. There is a subtle classification of the metastatic criteria of the lymph nodes which are often difficult to identify Axillary metastatic nodes are to be found in half the number of breast cancers.
Lymph node elastography has a 42% sensitivity. There is a significant number of false positives. The correct positioning of the elasticity box is essential in the case of small lymph node structures.
In the case of metastatic lymph nodes, elasticity is around 20–25 kPa.
A perfectly round lymph node without hyperechoic hilum is highly suspicious. To analyse it, it is important to make use of a Doppler examination.
A lymph node less than 2 mm large bears micro-metastases which will have but little influence on the evolution of the disease.
Lymph nodes larger than 3 mm or more bear macro-metastases which will modify significantly the general evolution of the patient.
90% of the metastatic nodes over 5 mm are thus analysed for an accurate pre-operative stage, with a significant saving of time, diagnostic accuracy and cost effectiveness.
The identification of the sentinel node is important if it can be carried out.
The taking of sample cells through fine needle aspiration or core biopsy makes it possible to assert there is an invasion of the lymph nodes, thus avoiding unnecessary complete axillary lympho-node dissection.
4.4 Better analysis of the zones of micro-calcifications detected through mammography
The vast majority of micro-calcifications are badly identified in echography. Elastography may allow a study of the zones targeted through the radiological examination as containing micro-calcifications. Ultrasound evidences the zones of intra-ductal or lobular epithelial proliferation (Figure 8).
Colour Doppler (ultra fast, angio-plus Doppler) coupled with 3D imagery allows a reconstruction of lobar anatomy with its possible pathological modifications, but it is obvious that it is impossible to distinguish simple epithelial proliferation from florid hyperplasia, from a case of CIS in situ or from a millimetric invasive cancer at its very beginning.
4.5 5 Prognostic study of a lesion and its aggressiveness
In 2011 and 2014, Evans was one of the pioneers in the description of the relationships between the size of the lesions, the increase in elasticity and the aggressiveness of the tumour, the contamination of the lymph nodes, the lympho-vascular invasion and the histological grade of the cancer [7, 8, 9, 10].
The hardest cancers are more invasive with a median value of 180 kPa and the highest histological grade. Median elasticity values of 126 kPa correspond to ductal cancers in situ. Benign lesions have a median score of 45 kPa. Lipomas have a score of 14 kPa, with 97% sensitivity and 88% specificity. These data can thus be considered as predictive (Figures 8 and 12).
4.6 Oncologic management and monitoring in the course of neoadjuvant chemotherapy
There is a significant link between the pre-operative elasticity values and the evolution of elasticity during the treatment, and this allows us to assess its efficiency. The decrease in elasticity and heterogenicity of the tumour corresponds to a good response to the treatment. Therapeutic monitoring is thus improved.
These results have proved to be more relevant than those achieved by dynamic MR with a contrasting agent, even though MR is considered as a golden rule in the monitoring of pre-operative therapy.
5. Practical information for the use of mammary elastography
5.1 Colour map code
The Hitachi company, a pioneer of strain elastography (SE) have expressed the modifications in the elasticity of mammary tissues through a colorimetric chart known as the ‘Tsukuba score’. Reds and yellows correspond to very supple tissues, green has a slightly higher elasticity score and blue a much increased gradient in elasticity; last of all, a deep blue zone surrounded with a pale blue halo is the sign of a lesion which is very likely to be malignant .
Another pioneer in Shear Wave Elastography (SWE), the Supersonic image group have chosen the opposite colour coding, red for a hard, probably malignant lesion, blue for low score, supple elasticity which is therefore benign. This latter, more ‘European’ colorimetric representation (red = danger) can very easily be reversed electronically through a simple modification in the software, and this applies to both SE and SWE techniques. This colour inversion is not a major difficulty for the user who, most of the time, does not use the two techniques simultaneously; he must simply make sure he follows some basic, standard rules (e.g. no hyper-pressure with the probe which must be strictly perpendicular to the skin, etc.) which he will have had fully described in the course of his training.
The use of a dual mode (mode B image joined to the elastography image in colour) enables a perfect synchronisation in the analysis of the lesion, either in SE or in SWE. The colour mode indicates very rapidly the suspicious (or non suspicious) character of an anomaly detected through echography .
As the appreciation of colours may vary from one user to another, the builders of these machines have turned towards more precise and measurable quantitative data.
The ‘fat to lesion ratio’ makes it possible to measure the variations in elasticity between the hardest tissues and the supplest fatty tissue with great precision.
The use of ROI (region of interest) or of the Q Box has to be well handled: one ROI/Q Box is positioned on the suspicious coloured lesion, the other is placed on the supplest possible tissue, generally the subcutaneous fatty tissue.
In SE, the ratio is graded from 1 to 10 (or more) with a ‘cut off point’ between 3 and 4 (lesion likely to be benign, or likely to be suspicious). In SWE the mean and standard deviations are provided in kPa (KiloPascal), ratio and averages derive from the quantitative measurements.
Evans has determined the threshold of 50 kPa for Birads 3 or below lesions which are benign as a rule. According to him, scores over 50/60 kPa correspond to Birads 4/5 lesions which are to be biopsied, scores higher than 100 kPa or more are a certainty of malignancy.
The most interesting case is that of the lesions graded Birads 3, when one keeps in mind that 2% in this category correspond to malignant lesions and that, furthermore, there exist ‘soft’ cancers (mucoid, colloid, in situ or no mass cancers). Mucinous cancers considered as ‘soft’ tumours reach high scores in SWE (from 95 to over 200 kPa). Quite obviously, one must take into account complementary factors such as the age of the patient, the size of the breast, the distance between the skin and the lesion, the fibrous or involuted character of the breast, all of which take their share in the Birads 3/4 scoring.
5.2 Regrading of these 3/4 Birads lesions = upgrade/downgrade:
Elastography allows to reduce the number of unnecessary biopsies through a better specificity and PPV (Positive Predictive Value). It guides the decision not to biopsy a Birads 4a lesion with a negative reassuring elastography and to suggest instead an echography follow-up 6 months later, or on the contrary, to biopsy a Birads 3 lesion with a suspicious elastography response. Such a way of dealing was presented by the Korean Society of Ultrasound (KSUM) in 2014 .
In the case of a negative Birads 3 lesion, the follow-up will be the same as for a Birads 2 lesion.
Negative Birads 4a = Birads 3
Positive Birads3 = Biopsy
Negative Birads 4a = Birads 2
5.3 Follow-up of treatment efficiency in a proven cancer
If mode B echography alone underestimates the size of the cancer, with the contribution of elastography, it produces a perfect assessment of the histological size of the lesion.
The prediction of the response to the neoadjuvant chemotherapy treatment has been studied by different groups who confirm that there is a relationship between the score of pre-operative elasticity and the response to the treatment.
The maximum score in elasticity of the tumour is related to its histological severity:
Invasive cancer elasticity score = between 140 and 180 kPa.
Ductal cancer in situ = between 70 and 180 kPa.
Benign lesion medium elasticity score = 45 kPa.
Lipoma = 15 kPa.
The 180 kPa is predictive of nodular metastasis. If information on the size of the tumour, the lymph node and vascular invasion and the histological grade of the cancer is added, capital information is obtained on the prognosis of the evolution of the cancer.
Modification of stiffness (up or down) seems to be a very relevant parameter to access treatment efficacy.
5.4 Assessment of echo graphically revealed micro-calcifications
Two conditions are to be faced: either micro-calcifications with an obvious focal lesion, or micro-calcifications without echo graphically visible lesions. A very small number only of these micro-calcifications can be detected through mode B echography. They are the indirect signs of an intra-ductal or intra-lobular disruption. In comparison to mammography, echography offers the added bonus to visualise directly the epithelial structure of the epithelial proliferation or hyperplasia type. Their development may correspond to a physiological character, an inflammation or a tumoral process. And it is only the bringing together of mode B echography, ultra fast Doppler, elastography and possibly 3D analysis, that allows to distinguish a probably benign lesion from a well-defined or a diffuse lesion, but it remains difficult, if not impossible, to distinguish between the successive stages in epithelial modifications: physiologic proliferation, florid hyperplasia, border line or cancer in situ in its earliest stages. The role of echography is to allow a selection of the patients at risks (with a thickening of epithelial structures) for whom follow-ups or further investigations must be considered.
5.5 Role of elastography in mammary pathology
The diagnosis of breast lesions and the way in which they are dealt with has progressed dramatically thanks to the use of new technologies in breast imaging. Among these techniques, ultrasound elastography has become an essential, unavoidable tool. It combines rapidity of execution, diagnostic reliability and remarkable reproducibility. It allows to put forward dubious cases and patients at risk who have to have regular check-ups. And it also allows a reduction in the high number of ultrasound false positives, a regular follow-up of probably benign lesions and a monitoring of the efficiency of neoadjuvant treatments .
At this stage, however, the study of lymph nodes invasion remains difficult and the understanding of the relationship between the maximum elasticity score of a tumour and its immuno-histological phenotype is not conclusive. Let us hope that future progress in echography will soon enable us to fill in these gaps.
The coupling of 3D Breast Echography + Angio-plus-Ultra-fast Colour Doppler with elastography has allowed significant improvements in evidencing the location of the breast lesions, their qualification and the management of pre-operative neoadjuvant chemotherapy. A better collaboration with the team who is in charge of the patient (surgeon, oncologist, doctor, radiotherapist, nurse etc.…) can thus be achieved to the patient’s greatest benefit.
In qualifying the grade of the tumour, the presence of metastases in the lymph nodes and in offering a prognosis linked to the aggressiveness of the tumour, the radiologist allows a significant saving of time for the therapeutic approach of the patient and a better targeted, more personalised therapy.
The evaluation of therapeutic care strategies is better adapted than a standard protocol. There are close relations between the modification of elasticity, the size of the tumour, the metastatic invasion of the lymph nodes, the more or less aggressive nature of the cancer and the choice of the suitable neoadjuvant chemotherapy.
The decrease in recall rate as well as in unnecessary punctures (40–50%) amounts to serious cost effectiveness.
Inter or intra-operator perfect reproducibility, fair possibility to repeat the examinations in over 85% of the cases and lastly outstanding sensitivity and specificity explain why the echography-elastography coupling has achieved a significant beneficial impact on breast imaging. Future developments are still to improve the diagnosis and follow up of breast cancer [10, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59, 60, 61, 62].
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