Breast Elastography

**81**

**Chapter 7**

**Abstract**

management?

ultrasound, BI-RADS

**1. Introduction**

**2. Epidemiology**

Strain Elastography in Invasive

*Angelica Rita Chiorean, Roxana Pintican, Diana Feier,* 

**Keywords:** breast cancer, invasive lobular carcinoma, elastography,

encountered type among invasive carcinomas.

Breast cancer remains the second cause of mortality in women, even if the mortality rates linked to it have drastically dropped at the present time. Based on the origin of the cancer cells, there are two types of breast cancer subtypes: ductal and lobular. Both include an "in situ" and an "invasive" form, depending on their extension to the neighboring tissues. We will further address invasive lobular cancer (ILC), which accounts for 5–15% of the breast cancers and is the second most

ILC has an estimated incidence of 2.7 per 100.000 people, with a mean diagnostic age higher than for invasive ductal carcinoma. About two-thirds of women are 55 or older at the time of the diagnosis, ILC tending to occur even later in life [1].

Breast cancer remains the second cause of mortality in women, even if the mortality rates linked to it have drastically dropped at the present time. Invasive lobular carcinoma (ILC) accounts for 5–15% of the breast cancers and it is the second most encountered type among invasive carcinomas. There has been reported a high rate for bilateral lesions (6–47%), multifocality/multicentricity (21%), all affecting ILC overall survival. Due to its nonspecific symptoms and to the fact that it does not invoke a vigorous desmoplastic response and has a low likelihood of producing calcifications, the ILC tends to be insidious on mammography. Contrast enhanced MRI has the lowest false negative rate in detecting ILC and it is the most accurate method of determining the lesion extension, though it is expensive and not widely available. Therefore, the ultrasound (US) plays a significant role in the diagnosis of ILC. US elastography imaging (EI) individualizes malignant breast lesions with high sensitivity and specificity. Recent studies suggested that US elastography can even diagnose lobular cancers that have benign findings on conventional imaging. Goal: present various US aspects and exemplify the added diagnostic value of strain elastography—how it may change the BIRADS category and further therapeutic

Lobular Carcinoma

*Dan Eniu and Maria Magdalena Duma*

#### **Chapter 7**

## Strain Elastography in Invasive Lobular Carcinoma

*Angelica Rita Chiorean, Roxana Pintican, Diana Feier, Dan Eniu and Maria Magdalena Duma*

#### **Abstract**

Breast cancer remains the second cause of mortality in women, even if the mortality rates linked to it have drastically dropped at the present time. Invasive lobular carcinoma (ILC) accounts for 5–15% of the breast cancers and it is the second most encountered type among invasive carcinomas. There has been reported a high rate for bilateral lesions (6–47%), multifocality/multicentricity (21%), all affecting ILC overall survival. Due to its nonspecific symptoms and to the fact that it does not invoke a vigorous desmoplastic response and has a low likelihood of producing calcifications, the ILC tends to be insidious on mammography. Contrast enhanced MRI has the lowest false negative rate in detecting ILC and it is the most accurate method of determining the lesion extension, though it is expensive and not widely available. Therefore, the ultrasound (US) plays a significant role in the diagnosis of ILC. US elastography imaging (EI) individualizes malignant breast lesions with high sensitivity and specificity. Recent studies suggested that US elastography can even diagnose lobular cancers that have benign findings on conventional imaging. Goal: present various US aspects and exemplify the added diagnostic value of strain elastography—how it may change the BIRADS category and further therapeutic management?

**Keywords:** breast cancer, invasive lobular carcinoma, elastography, ultrasound, BI-RADS

#### **1. Introduction**

Breast cancer remains the second cause of mortality in women, even if the mortality rates linked to it have drastically dropped at the present time. Based on the origin of the cancer cells, there are two types of breast cancer subtypes: ductal and lobular. Both include an "in situ" and an "invasive" form, depending on their extension to the neighboring tissues. We will further address invasive lobular cancer (ILC), which accounts for 5–15% of the breast cancers and is the second most encountered type among invasive carcinomas.

#### **2. Epidemiology**

ILC has an estimated incidence of 2.7 per 100.000 people, with a mean diagnostic age higher than for invasive ductal carcinoma. About two-thirds of women are 55 or older at the time of the diagnosis, ILC tending to occur even later in life [1].

#### **3. Pathology and ILC subtypes**

The tumor develops at the terminal ductal-lobular unit (TDLU), and it is composed of cancer cells that are individually dispersed or arranged in a single-file pattern. Often, the cells form a target-like configuration around normal breast ducts. Two main histology findings are characteristic for invasive lobular cancer: the noncohesive cell pattern and the minimal desmoplastic response. The first is an effect of the E-cadherin (CDH1) germline mutation encountered in about 85% of the tumors, which results in the loss of adhesion proteins and a discohesive morphologic pattern [2]. The second is due to the fact that malignant cells grow in the mammary stroma and adipose tissue and induce less desmoplastic reaction than ductal carcinoma, which has important repercussions on the imaging aspects [3].

As it regards the ILC subtypes, occasionally the classic single-file formation is absent, and there is a different pattern encountered: solid (large sheets with little stroma), alveolar (groups of 20 cells), or tubular-lobular (tubelike structures together with single-file pattern) [2, 3].

The classic ILC presents with tumor cells that are usually small, uniform, and round with minimal pleomorphism. Otherwise, a less often subtype cell might be reported: pleomorphic or signet-ring cells.

The majority of ILC are positive for estrogen and progesterone receptors and are negative for the HER2 amplification (consistent with a luminal A category).

#### **4. Signs and symptoms**

The invasive lobular carcinoma may be asymptomatic. Due to the typical spread pattern, some of the patients may present with the first sign of ILC as a skin thickening or hardening of the breast rather than a distinct lump. Basically there are no ILC-specific signs or symptoms; the patients' physical examination may reveal general breast cancerrelated changes such as a swelling area, skin irritation or dimpling, breast or nipple pain, nipple discharge (other than breast milk), and even an axillary lump [4].

Due to the lack and nonspecific symptoms, up to 10% of the patients present with metastatic disease at the time of diagnosis [1].

#### **5. Diagnosis of ILC**

Breast cancer in general might be diagnosed using different complementary methods or techniques, starting with a physical breast examination; whether we are using screening or diagnostic mammography (Mx), ultrasound, or magnetic resonance (MRI), it is well known that imaging often underestimates this disease's extension. The tissue analysis remains the gold standard for tumor diagnostic, regardless if the tumor tissue originates from a biopsy or a surgical excision.

Regarding the tumor appearance, a high rate for bilateral lesions (6–47%) has been reported, multifocality/multicentricity (21%), all affecting the ILC overall survival (**Figure 1**) [1].

#### **5.1 Mammography**

The sensitivity of mammography is reported to be lower for ILC than for invasive ductal carcinoma, ranging from 34–72%, and it is frequently seen in only one view (often on cranio-caudal compared to mediolateral oblique) [5]. Most commonly, the tumor presents as a spiculated mass lesion without calcifications.

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**Figure 2.**

*Strain Elastography in Invasive Lobular Carcinoma DOI: http://dx.doi.org/10.5772/intechopen.88077*

benign lesions (**Figure 2**).

hyperechoic halo (**Figure 3**).

**5.2 Ultrasound**

**Figure 1.**

*5.2.1 B-mode*

fence (**Figure 4**).

In some cases, architectural distortions or asymmetrical densities are observed; moreover, up to 16% of ILC remains mammographically occult or are attributed to

*Multifocal ILC. Ultrasound suspect lesions located in the right breast, first at 11 o'clock (A) and second at 9 o'clock (B).*

The studies reported a sensibility of 98% in the ultrasound diagnostic of ILC [6]. The tumor usually presents as a hypoechoic mass, with ill-defined margins and posterior acoustic shadowing (58%), occasionally without shadowing (27%) [6]. Contrary to ductal carcinoma, which commonly presents as a lesion perpendicular to the surface, ILC may exhibit a so-called "wider than tall" shape, a tumor that is parallel to the skin. In some cases, the mass might be heterogeneous with an iso- or

Two classic signs of ILC were described using B-mode of ultrasound. First, the Golden Gate sign resulted from 2 to 3 adjacent Cooper's ligaments involved by cancer so that the shadowing area (hypoechoic area) resembles the shape of a suspension bridge seen from the profile. The second one, named the picket fence sign, is observed when more numerous and more closely spaced Cooper's ligaments are involved in cancer and the shadowing area resembles the profile of a picket

*Subtle ILC mammographic findings: An asymmetry of density is seen on the CC view (B, arrow), without a correspondent on MLO projection (A). Note the same density of the lesion as of the normal tissue breast. The ultrasound (CD) revealed a 5 mm, spiculated, hypoechoic lesion with vascularization on color Doppler.*

*Strain Elastography in Invasive Lobular Carcinoma DOI: http://dx.doi.org/10.5772/intechopen.88077*

**Figure 1.** *Multifocal ILC. Ultrasound suspect lesions located in the right breast, first at 11 o'clock (A) and second at 9 o'clock (B).*

In some cases, architectural distortions or asymmetrical densities are observed; moreover, up to 16% of ILC remains mammographically occult or are attributed to benign lesions (**Figure 2**).

#### **5.2 Ultrasound**

*Ultrasound Elastography*

**3. Pathology and ILC subtypes**

together with single-file pattern) [2, 3].

reported: pleomorphic or signet-ring cells.

**4. Signs and symptoms**

**5. Diagnosis of ILC**

survival (**Figure 1**) [1].

**5.1 Mammography**

The tumor develops at the terminal ductal-lobular unit (TDLU), and it is composed of cancer cells that are individually dispersed or arranged in a single-file pattern. Often, the cells form a target-like configuration around normal breast ducts. Two main histology findings are characteristic for invasive lobular cancer: the noncohesive cell pattern and the minimal desmoplastic response. The first is an effect of the E-cadherin (CDH1) germline mutation encountered in about 85% of the tumors, which results in the loss of adhesion proteins and a discohesive morphologic pattern [2]. The second is due to the fact that malignant cells grow in the mammary stroma and adipose tissue and induce less desmoplastic reaction than ductal carcinoma, which has important repercussions on the imaging aspects [3]. As it regards the ILC subtypes, occasionally the classic single-file formation is absent, and there is a different pattern encountered: solid (large sheets with little stroma), alveolar (groups of 20 cells), or tubular-lobular (tubelike structures

The classic ILC presents with tumor cells that are usually small, uniform, and round with minimal pleomorphism. Otherwise, a less often subtype cell might be

The majority of ILC are positive for estrogen and progesterone receptors and are

The invasive lobular carcinoma may be asymptomatic. Due to the typical spread pattern, some of the patients may present with the first sign of ILC as a skin thickening or hardening of the breast rather than a distinct lump. Basically there are no ILC-specific signs or symptoms; the patients' physical examination may reveal general breast cancerrelated changes such as a swelling area, skin irritation or dimpling, breast or nipple pain,

Due to the lack and nonspecific symptoms, up to 10% of the patients present

Breast cancer in general might be diagnosed using different complementary methods or techniques, starting with a physical breast examination; whether we are using screening or diagnostic mammography (Mx), ultrasound, or magnetic resonance (MRI), it is well known that imaging often underestimates this disease's extension. The tissue analysis remains the gold standard for tumor diagnostic, regardless if the tumor tissue originates from a biopsy or a surgical excision.

Regarding the tumor appearance, a high rate for bilateral lesions (6–47%) has been reported, multifocality/multicentricity (21%), all affecting the ILC overall

The sensitivity of mammography is reported to be lower for ILC than for invasive ductal carcinoma, ranging from 34–72%, and it is frequently seen in only one view (often on cranio-caudal compared to mediolateral oblique) [5]. Most commonly, the tumor presents as a spiculated mass lesion without calcifications.

negative for the HER2 amplification (consistent with a luminal A category).

nipple discharge (other than breast milk), and even an axillary lump [4].

with metastatic disease at the time of diagnosis [1].

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The studies reported a sensibility of 98% in the ultrasound diagnostic of ILC [6]. The tumor usually presents as a hypoechoic mass, with ill-defined margins and posterior acoustic shadowing (58%), occasionally without shadowing (27%) [6]. Contrary to ductal carcinoma, which commonly presents as a lesion perpendicular to the surface, ILC may exhibit a so-called "wider than tall" shape, a tumor that is parallel to the skin. In some cases, the mass might be heterogeneous with an iso- or hyperechoic halo (**Figure 3**).

#### *5.2.1 B-mode*

Two classic signs of ILC were described using B-mode of ultrasound. First, the Golden Gate sign resulted from 2 to 3 adjacent Cooper's ligaments involved by cancer so that the shadowing area (hypoechoic area) resembles the shape of a suspension bridge seen from the profile. The second one, named the picket fence sign, is observed when more numerous and more closely spaced Cooper's ligaments are involved in cancer and the shadowing area resembles the profile of a picket fence (**Figure 4**).

#### **Figure 2.**

*Subtle ILC mammographic findings: An asymmetry of density is seen on the CC view (B, arrow), without a correspondent on MLO projection (A). Note the same density of the lesion as of the normal tissue breast. The ultrasound (CD) revealed a 5 mm, spiculated, hypoechoic lesion with vascularization on color Doppler.*

#### **Figure 3.**

*ILC presented as a heterogeneous mass, with small cystic areas included and ill-defined margins (A), vascularized on color Doppler (B). Note the mass orientation, parallel to the surface, with a "wider than tall" appearance.*

**Figure 4.** *Classic sign of ILC: Golden Gate bridge (A) and picket fence (B).*

#### *5.2.2 Doppler mode*

The Doppler mode highlights the presence of the blood vessels within the tumor, whether it is a mild, moderate, or intensely vascularized tumor mass. The vessel's spreading pattern is not characteristic, usually the tumor presenting with diffusely distributed vascularization. Rarely, a malignant mass may present as an avascular tumor, due to the present-day limitation of the technique (vessels too small to be highlighted).

#### *5.2.3 Elastography*

In breast ultrasound, both strain (static) and shear wave (dynamic) elastography are used. Ultrasound elastography of the ILC masses exhibits various patterns, from soft to mosaic and predominantly hard tumors. Tsukuba score (TS) is often used to qualitatively classify the elasticity of the masses, from 1 (soft) to 5 (extensively hard lesions) (**Table 1**).

The elasticity varies between different lobular cancer masses, which may even have an elastography score similar with the normal adjacent breast tissue. An important take-home message lies in the lesion's grayscale aspect: if the B-mode indicates any sign of malignancy, a normal hardness should not delay the following biopsy.

ILC commonly presents as hard masses (Tsukuba 4 or 5 score). Sometimes a mosaic pattern might be obtained, and rarely a blue-green-red (BGR) appearance may be noted.

A topic of interest nowadays is represented by the US prediction regarding the breast cancer tumor grades. The mean elasticity/B-mode ratio was reported as statistically different between ILC and grade III ductal carcinoma, versus mucinous or grade I and II ductal cancers [7].

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**Table 1.**

On the topic of shear wave elastography, the method provides a quantitative assessment and tissue stiffness values, represented in kilopascals (kPa). A value higher than 45.7 kPa for the mean elasticity was attributed to malignant breast tumors (**Figure 5**) [8].

*Tsukuba qualitative score. The left column displays the elastography score, the middle column shows the elastography/B-mode appearances, and the right column describes the score meaning. All the abovementioned* 

*Strain Elastography in Invasive Lobular Carcinoma DOI: http://dx.doi.org/10.5772/intechopen.88077*

Benign

Benign

Probably benign

Malignant

Malignant

Benign/cyst/ malignant with necrotic area

Score 1 Complete

Score 2

areas

Score 3 Central stiff area with peripheral deformability

Score 4

Score 5 Stiff lesion and surrounding area

BGR sign

Blue-green-red pattern

*lesions were proven to be invasive lobular cancers.*

Completely stiff lesion

deformability of lesion

Lesion with little stiff

*Ultrasound Elastography*

**84**

**Figure 4.**

**Figure 3.**

*appearance.*

*5.2.2 Doppler mode*

*5.2.3 Elastography*

lesions) (**Table 1**).

the following biopsy.

or grade I and II ductal cancers [7].

*Classic sign of ILC: Golden Gate bridge (A) and picket fence (B).*

The Doppler mode highlights the presence of the blood vessels within the tumor, whether it is a mild, moderate, or intensely vascularized tumor mass. The vessel's spreading pattern is not characteristic, usually the tumor presenting with diffusely distributed vascularization. Rarely, a malignant mass may present as an avascular tumor, due to the present-day limitation of the technique (vessels too small to be highlighted).

*ILC presented as a heterogeneous mass, with small cystic areas included and ill-defined margins (A), vascularized on color Doppler (B). Note the mass orientation, parallel to the surface, with a "wider than tall"* 

In breast ultrasound, both strain (static) and shear wave (dynamic) elastography are used. Ultrasound elastography of the ILC masses exhibits various patterns, from soft to mosaic and predominantly hard tumors. Tsukuba score (TS) is often used to qualitatively classify the elasticity of the masses, from 1 (soft) to 5 (extensively hard

The elasticity varies between different lobular cancer masses, which may even have an elastography score similar with the normal adjacent breast tissue. An important take-home message lies in the lesion's grayscale aspect: if the B-mode indicates any sign of malignancy, a normal hardness should not delay

ILC commonly presents as hard masses (Tsukuba 4 or 5 score). Sometimes a mosaic pattern might be obtained, and rarely a blue-green-red (BGR) appearance may be noted. A topic of interest nowadays is represented by the US prediction regarding the breast cancer tumor grades. The mean elasticity/B-mode ratio was reported as statistically different between ILC and grade III ductal carcinoma, versus mucinous


#### **Table 1.**

*Tsukuba qualitative score. The left column displays the elastography score, the middle column shows the elastography/B-mode appearances, and the right column describes the score meaning. All the abovementioned lesions were proven to be invasive lobular cancers.*

On the topic of shear wave elastography, the method provides a quantitative assessment and tissue stiffness values, represented in kilopascals (kPa). A value higher than 45.7 kPa for the mean elasticity was attributed to malignant breast tumors (**Figure 5**) [8].

#### **Figure 5.**

*Breast elastography techniques. (A) Vascularized lesion, hard on strain elastography. (B) Vascularized area, soft on shear wave elastography. Note the difference between stiffness' color coding: Blue in strain EI = hard, blue in share wave EI = soft.*

A comparison of strain and shear wave ultrasound elastography in differentiating benign and malignant breast lesions concluded that strain ultrasound elastography is more specific (93.7%) and less sensitive (81.7%), while shear wave ultrasound elastography is more sensitive (95.8%) and less specific (84.8%) in differentiating benign from malignant breast lesions [9].

There are three additional and important EI key aspects that help in the ILC diagnostic:


To conclude, whether or not it is a strain or a shear wave, elastography methods are adding value to the ILC diagnostic and should be definitely used in the assessment of every patient. Moreover, it may change the BI-RADS category from a probable benign lesion (score 3) to a suspicious lesion (score 4). Thereby, elastography has an important impact in the patient's therapeutic management, which translates in certain cases, in switching from a short-time follow-up to biopsy.

By educational purposes, all ultrasound characteristics presented above will be highlighted in the following case-based section. The various ILC imaging appearances were grouped in subcategories, as it follows:

a.Hypoechoic mass with posterior acoustic shadowing (**Figure 6**).

b.Hypoechoic mass without posterior acoustic shadowing (**Figure 7**).

c.Architectural distortion (**Figures 8** and **9**).


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p < 0.001) (**Figure 15**) [13].

*Strain Elastography in Invasive Lobular Carcinoma DOI: http://dx.doi.org/10.5772/intechopen.88077*

**Figure 6.**

**Figure 7.**

**Figure 8.**

*hard on elastography (C, TS 5).*

*(B), and hard on elastography (C, TS 5).*

f. Well-defined nodule. Studies reported up to 2–12% of the ILC cases as a

*ILC lesion presents as an architectural distortion with mild posterior acoustic shadowing, hardly visible on* 

detected during a second-look US after an MRI depiction (**Figure 14**).

h.Axillary abnormality. Regarding the US sensitivity in the metastasis detection, the technique was reported positive in about 50% of the N1 cases. Furthermore, US is able to exclude 96% of the N2 and N3 axillary metastasis (more than four positive lymph nodes). The fine needle biopsy is less sensitive in ILC than invasive ductal carcinoma (IDC vs. ILC; 98.4% vs. 53.6%;

g.Occult lesion. Not often, ILC may not be highlighted by ultrasound. Authors report up to 10% of the cases missed on US [12]. Sometimes, a lesion might be

*ILC lesion presents as a hypoechoic mass with intense posterior acoustic shadowing (A), vascularized (B), and* 

*ILC lesion presents as an ill-defined, hypoechoic mass without posterior acoustic shadowing (A), hypovascular* 

pseudo-benign, well-defined nodule (**Figure 13**) [12].

*grayscale (A). The area is hypovascular (B) and hard on elastography (C, TS 4).*

#### **Figure 6.**

*Ultrasound Elastography*

*blue in share wave EI = soft.*

diagnostic:

**Figure 5.**

A comparison of strain and shear wave ultrasound elastography in differentiating benign and malignant breast lesions concluded that strain ultrasound elastography is more specific (93.7%) and less sensitive (81.7%), while shear wave ultrasound elastography is more sensitive (95.8%) and less specific (84.8%) in dif-

*Breast elastography techniques. (A) Vascularized lesion, hard on strain elastography. (B) Vascularized area, soft on shear wave elastography. Note the difference between stiffness' color coding: Blue in strain EI = hard,* 

There are three additional and important EI key aspects that help in the ILC

1.Highlighting hardly visible lesions—Sometimes a breast lesion might be isoechoic to the surrounding breast tissue, scarcely visible in grayscale; in some cases elastography may help us in identifying those hard lesions with greater confidence (the lesions will appear as isoechoic on B-mode and blue on strain EI).

2.Identifying pseudo-benign lesions—EI may indicate lobular cancers that have benign or normal findings on conventional imaging as suspicious [10].

To conclude, whether or not it is a strain or a shear wave, elastography methods are adding value to the ILC diagnostic and should be definitely used in the assessment of every patient. Moreover, it may change the BI-RADS category from a probable benign lesion (score 3) to a suspicious lesion (score 4). Thereby, elastography has an important impact in the patient's therapeutic management, which translates

By educational purposes, all ultrasound characteristics presented above will be highlighted in the following case-based section. The various ILC imaging appear-

in certain cases, in switching from a short-time follow-up to biopsy.

a.Hypoechoic mass with posterior acoustic shadowing (**Figure 6**).

d.Iso- or hypoechoic area or non-mass lesion (**Figures 10** and **11**).

e.Hyperechoic lesion. Even if the hyperechoic appearance usually represents a benign entity, up to 5% of the ILC were reported as hyperechoic lesions, out of which 48% were associated with posterior acoustic shadowing (**Figure 12**) [11].

b.Hypoechoic mass without posterior acoustic shadowing (**Figure 7**).

ances were grouped in subcategories, as it follows:

c.Architectural distortion (**Figures 8** and **9**).

3.Suggesting a larger lesion—It is known that imaging often underestimates ILC. Even so, EI may sometimes suggest a lesion's extension by highlighting a hard area that exceeds the grayscale lesion (lesions with Tsukuba 5 score).

ferentiating benign from malignant breast lesions [9].

**86**

*ILC lesion presents as a hypoechoic mass with intense posterior acoustic shadowing (A), vascularized (B), and hard on elastography (C, TS 5).*

#### **Figure 7.**

*ILC lesion presents as an ill-defined, hypoechoic mass without posterior acoustic shadowing (A), hypovascular (B), and hard on elastography (C, TS 5).*

#### **Figure 8.**

*ILC lesion presents as an architectural distortion with mild posterior acoustic shadowing, hardly visible on grayscale (A). The area is hypovascular (B) and hard on elastography (C, TS 4).*


#### **Figure 9.**

*Hardly visible ILC isoechoic lesion (A) associated with a hypovascular architectural distortion (B). The lesion is easily spotted on elastography, as a hard area (C, TS 4).*

#### **Figure 10.**

*Hypoechoic area with hyperechoic halo resembling the picket fence sign (A), with minimal vascularization on color Doppler (B). The core needle biopsy (C) revealed an ILC lesion, with positive estrogen and progesterone receptors RE = 100%, RP = 25%, Ki67 = 15%, and HER2 negative.*

#### **Figure 11.**

*Hypoechoic, hypovascular area which presents with mild posterior acoustic shadowing (AC). Note that the hard area is larger on elastography than grayscale (B, TS 5).*

#### **Figure 12.**

*Hyperechoic, ill-defined lesion (A), apparently avascular (B), but hard on elastography (C, TS 4). At the time of diagnosis, the patient presented peritoneal metastasis.*

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*Strain Elastography in Invasive Lobular Carcinoma DOI: http://dx.doi.org/10.5772/intechopen.88077*

*higher BI-RADS 4b score. The core needle biopsy showed an ILC relapse.*

**Figure 13.**

**Figure 14.**

**Figure 15.**

*biopsy concluded an ILC metastasis.*

i.ILC with BGR appearance. Rarely, ILC may display a blue-green-red sign due to a necrotic component. Even if the BGR sign is commonly attributed to cysts, its presence in a solid, suspicious mass may never delay a biopsy (**Figure 16**).

*The mammography shows a highly dense right breast and an abnormal axillary mass (A, arrow). The US revealed an enlarged, rounded lymph node (B), with intense and chaotic vascularization (C). The core needle* 

*A patient with a history of ILC treated with mastectomy 24 years ago. The present US revealed a well-defined, hypoechoic nodule in the area of mastectomy (A). The nodule is intensely vascularized (B) and hard on elastography (C, TS 4). Initially considered a BI-RADS 4a lesion, after EI the lesion has been assigned to a* 

*A breast lesion with suspect features was detected at US and proven to be an ILC (AB). The following staging* 

*MRI highlighted not one, but two lesions (C), concluding that one of the lesions was US occult.*

j.ILC lesions in which elastography changed the BI-RADS score. It was previously established that in order to achieve an accurate breast cancer diagnosis, US B-mode should be combined with Color Doppler and elastography. Regarding EI, there was a positive impact in breast cancer diagnosis, especially for small lesions [14]. Moreover, in invasive lobular cancer, EI demonstrated to improve the BI-RADS classification, particularly for lesions smaller than 13 mm (**Figures 17**–**19**) [15].

#### **Figure 13.**

*Ultrasound Elastography*

**Figure 9.**

**Figure 10.**

**Figure 11.**

*is easily spotted on elastography, as a hard area (C, TS 4).*

*receptors RE = 100%, RP = 25%, Ki67 = 15%, and HER2 negative.*

*hard area is larger on elastography than grayscale (B, TS 5).*

*of diagnosis, the patient presented peritoneal metastasis.*

*Hardly visible ILC isoechoic lesion (A) associated with a hypovascular architectural distortion (B). The lesion* 

*Hypoechoic area with hyperechoic halo resembling the picket fence sign (A), with minimal vascularization on color Doppler (B). The core needle biopsy (C) revealed an ILC lesion, with positive estrogen and progesterone* 

*Hypoechoic, hypovascular area which presents with mild posterior acoustic shadowing (AC). Note that the* 

*Hyperechoic, ill-defined lesion (A), apparently avascular (B), but hard on elastography (C, TS 4). At the time* 

**88**

**Figure 12.**

*A patient with a history of ILC treated with mastectomy 24 years ago. The present US revealed a well-defined, hypoechoic nodule in the area of mastectomy (A). The nodule is intensely vascularized (B) and hard on elastography (C, TS 4). Initially considered a BI-RADS 4a lesion, after EI the lesion has been assigned to a higher BI-RADS 4b score. The core needle biopsy showed an ILC relapse.*

#### **Figure 14.**

*A breast lesion with suspect features was detected at US and proven to be an ILC (AB). The following staging MRI highlighted not one, but two lesions (C), concluding that one of the lesions was US occult.*

#### **Figure 15.**

*The mammography shows a highly dense right breast and an abnormal axillary mass (A, arrow). The US revealed an enlarged, rounded lymph node (B), with intense and chaotic vascularization (C). The core needle biopsy concluded an ILC metastasis.*


#### **Figure 16.**

*Intensely hypoechoic nodule with partially well-defined, partially ill-defined margins (A), moderately vascularized on color Doppler examination (B). The elastography displays a blue-green-red appearance (C). Core biopsy revealed an ILC lesion.*

#### **Figure 17.**

*BI-RADS 3 to BI-RADS 4a. ILC presented as a small hypoechoic lesion with indistinct margins (A), hypovascular (B), and hard aspect on EI (C, TS 4/5). The lesion was upgraded from BI-RADS 3 to BI-RADS 4a after the elastography criterion was added.*

#### **Figure 18.**

*BI-RADS 4a to BI-RADS 4b. A small, avascular, hyperechoic lesion with indistinct margins (A) and hard on EI (B, TS 4). The core needle biopsy revealed ILC (C). The lesion was upgraded from BI-RADS 4a to BI-RADS 4b after the elastography criterion was added.*

#### **Figure 19.**

*Doppler US reveals a hypoechoic round lesion with partially angulated margins and peripheral vascularity (A). On strain elastography (B), the entire lesion and its surrounding parenchyma were shaded blue (TS 5). The lesion was upgraded from BI-RADS 4B to BI-RADS 4C after the elastography criterion was added.*

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**7. Conclusion**

**Acknowledgements**

**5.3 MRI**

**Figure 20.**

(plateau) curve (**Figure 20**).

**6. Treatment and prognosis**

positive resection margins are common.

the patient's therapeutic management.

*Strain Elastography in Invasive Lobular Carcinoma DOI: http://dx.doi.org/10.5772/intechopen.88077*

Due to its propensity for bilaterality and multicentricity, breast MRI is usually recommended when histology of a lesion reveals an ILC. MRI easily highlights occult Mx and US lesions and has the lowest false-negative rate in detecting ILC [16]. In addition, MRI has the highest accuracy in measuring ILC sizes, whether it is a mass or non-mass enhancement pattern. ILC kinetic is rarely a type III curve (washout) or type I curve, more often displaying a type II

*Heterogeneous US area of ILC, which is moderately vascularized and hard on elastography (AB, TS 5). The MRI (C) shows a non-mass enhancement, with a regional distribution, larger than the area predicted on US.*

Depending on the disease's stage, there is a local ILC treatment represented by surgery and radiation therapy and a systemic treatment characterized by chemotherapy, hormonal therapy, or targeted therapies. Due to its diffuse invasive nature,

ILC spreads slowly outside the breast, but when it does, it tends to manifests with atypical metastases, affecting the gastrointestinal tract (as a diffuse spreading process of the colon 26%, stomach, or small bowel), ovaries (21%), peritoneum (as Krukenberg syndrome, 30%), retroperitoneum, leptomeningeal, or

Despite the multifocality, the bilateral lesions, and the atypical metastases, the prognosis for ILC patients with a given size and stage is believed to be slightly

The ultrasound plays a significant role in the diagnosis of invasive lobular carcinoma. Ultrasound elastography imaging individualizes malignant breast lesions with high sensitivity and specificity, being sometimes a "problem-solving" method. Moreover, it may change the BI-RADS category and have an important impact on

bone. It may also cause lymph node, lung, or liver metastasis.

higher than for patients with invasive ductal carcinoma.

There are no acknowledgments nor funding sources.

#### **Figure 20.**

*Ultrasound Elastography*

**Figure 16.**

**Figure 17.**

**Figure 18.**

*Core biopsy revealed an ILC lesion.*

*4a after the elastography criterion was added.*

*BI-RADS 4b after the elastography criterion was added.*

*Intensely hypoechoic nodule with partially well-defined, partially ill-defined margins (A), moderately vascularized on color Doppler examination (B). The elastography displays a blue-green-red appearance (C).* 

*BI-RADS 3 to BI-RADS 4a. ILC presented as a small hypoechoic lesion with indistinct margins (A), hypovascular (B), and hard aspect on EI (C, TS 4/5). The lesion was upgraded from BI-RADS 3 to BI-RADS* 

*BI-RADS 4a to BI-RADS 4b. A small, avascular, hyperechoic lesion with indistinct margins (A) and hard on EI (B, TS 4). The core needle biopsy revealed ILC (C). The lesion was upgraded from BI-RADS 4a to* 

*Doppler US reveals a hypoechoic round lesion with partially angulated margins and peripheral vascularity (A). On strain elastography (B), the entire lesion and its surrounding parenchyma were shaded blue (TS 5). The lesion was upgraded from BI-RADS 4B to BI-RADS 4C after the elastography criterion was added.*

**90**

**Figure 19.**

*Heterogeneous US area of ILC, which is moderately vascularized and hard on elastography (AB, TS 5). The MRI (C) shows a non-mass enhancement, with a regional distribution, larger than the area predicted on US.*

#### **5.3 MRI**

Due to its propensity for bilaterality and multicentricity, breast MRI is usually recommended when histology of a lesion reveals an ILC. MRI easily highlights occult Mx and US lesions and has the lowest false-negative rate in detecting ILC [16]. In addition, MRI has the highest accuracy in measuring ILC sizes, whether it is a mass or non-mass enhancement pattern. ILC kinetic is rarely a type III curve (washout) or type I curve, more often displaying a type II (plateau) curve (**Figure 20**).

#### **6. Treatment and prognosis**

Depending on the disease's stage, there is a local ILC treatment represented by surgery and radiation therapy and a systemic treatment characterized by chemotherapy, hormonal therapy, or targeted therapies. Due to its diffuse invasive nature, positive resection margins are common.

ILC spreads slowly outside the breast, but when it does, it tends to manifests with atypical metastases, affecting the gastrointestinal tract (as a diffuse spreading process of the colon 26%, stomach, or small bowel), ovaries (21%), peritoneum (as Krukenberg syndrome, 30%), retroperitoneum, leptomeningeal, or bone. It may also cause lymph node, lung, or liver metastasis.

Despite the multifocality, the bilateral lesions, and the atypical metastases, the prognosis for ILC patients with a given size and stage is believed to be slightly higher than for patients with invasive ductal carcinoma.

#### **7. Conclusion**

The ultrasound plays a significant role in the diagnosis of invasive lobular carcinoma. Ultrasound elastography imaging individualizes malignant breast lesions with high sensitivity and specificity, being sometimes a "problem-solving" method. Moreover, it may change the BI-RADS category and have an important impact on the patient's therapeutic management.

#### **Acknowledgements**

There are no acknowledgments nor funding sources.

*Ultrasound Elastography*

### **Conflict of interest**

All authors declare no conflict of interest.

#### **Notes/thanks/other declarations**

We would like to thank our families for the support and understanding.

### **Author details**

Angelica Rita Chiorean1,2\*, Roxana Pintican3 , Diana Feier1,2, Dan Eniu1,4 and Maria Magdalena Duma<sup>5</sup>

1 "Iuliu Hațieganu" University of Medicine and Pharmacy, Cluj-Napoca, Romania

2 Medimages Breast Center, Cluj-Napoca, Romania

3 Department of Radiology and Medical Imaging, County Hospital, Cluj-Napoca, Romania

4 "Prof. Dr. Ion Chiricuță" Oncology Institute, Surgery Department, Cluj-Napoca, Romania

5 Micromedica Clinic, Piatra-Neamț, Romania

\*Address all correspondence to: chiorean\_angi@yahoo.com

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

**93**

*Strain Elastography in Invasive Lobular Carcinoma DOI: http://dx.doi.org/10.5772/intechopen.88077*

[1] Invasive Lobular Cancer. [Internet].

strain ultrasound elastography in the differentiation of benign and malignant breast lesions. AJR. American Journal of Roentgenology. 2013;**201**:347-356. DOI:

Whelehan P, Thomson K, Evans A. Value of shear-wave elastography in the diagnosis of symptomatic invasive lobular breast cancer. Clinical Radiology. 2015;**70**:604-609. DOI:

[11] Jones KN, Magut M, Henrichsen TL, Boughey JC, Reynolds C, Glazebrook

[12] Johnson K, Sarma D, Hwang ES. Lobular breast cancer series: Imaging. Breast Cancer Research. 2015;**17**:94. DOI: 10.1186/s13058-015-0605-0

[13] Topps A, Clay V, Absar M, Howe M, Lim Y, Johnson R, et al. The sensitivity of pre-operative axillary staging in breast cancer: Comparison of invasive lobular and ductal carcinoma. European Journal of Surgical Oncology.

2014;**40**:813-817. DOI: 10.1016/j.

[14] Botticeli A, Mazzotti E, Di Stefano D, et al. Positive impact of elastography in breast cancer diagnosis: An institutional experience. Journal of Ultrasound. 2015;**18**:321-327. DOI:

10.1007/s40477-015-0177-y

[15] Chiorean A, Szep M, Feier D, et al. Impact of strain Elastography on BI-RADS classification in small invasive lobular carcinoma. Medical Ultrasonography. 2018;**20**:148-153. DOI:

ejso.2014.03.026

10.11152/mu-1272

10.2214/AJR.12.10416

[10] Sim YT, Vinnicombe S,

10.1016/j.crad.2015.02.004

KN. Pure lobular carcinoma of the breast presenting as a hyperechoic mass: Incidence and imaging characteristics. AJR. 2013;**201**:W765-W769. DOI: 10.2214/

AJR.12.9742

breastcancer.org/symptoms/types/ilc

[2] Srivastava S. Breast Malignant, Males, Children [Internet]. 2017. Available from: http://www. pathologyoutlines.com/topic/ breastmalignantlcis.html [Accessed:

[3] Jones KN, Magut M, Henrichsen TL, et al. Pure lobular carcinoma of the breast presenting as a hyperechoic mass: Incidence and imaging characteristics.

Roentgenology. 2013;**201**:W765-W769.

[4] Breast Cancer Signs and Symptoms online. Available at: https://www.cancer. org/cancer/breast-cancer/about/breastcancer-signs-and-symptoms.html

[5] Berg WA, Birdwell RL. Diagnostic Imaging Breast. Salt Lake City: Amyrsis;

[6] Selinko VL, Middleton LP, Dempsey PJ. Role of sonography in diagnosing and staging invasive lobular carcinoma.

2004;**32**:323-332. DOI: 10.1002/jcu.20052

[7] Grajo JR, Barr RG. Strain elastography for prediction of breast cancer tumor grades. Journal of Ultrasound in Medicine. 2014;**33**:129-134. DOI:

[8] Olgun DÇ, Korkmazer B, Kılıç F, et al. Use of shear wave elastography to differentiate benign and malignant

[9] Chang JM, Won JK, Lee KB, et al. Comparison of shear-wave and

breast lesions. Diagnostic and Interventional Radiology. 2014;**20**: 239-244. DOI: 10.5152/dir.2014.13306

Journal of Clinical Ultrasound.

Available from: http://www.

[Accessed: 20 May 2019]

AJR. American Journal of

DOI: 10.2214/AJR.12.9742

[Accessed: 20 May 2019]

2006. pp. 144-147

10.7863/ultra.33.1.129

**References**

20 May 2019]

*Strain Elastography in Invasive Lobular Carcinoma DOI: http://dx.doi.org/10.5772/intechopen.88077*

#### **References**

*Ultrasound Elastography*

**Conflict of interest**

All authors declare no conflict of interest.

**Notes/thanks/other declarations**

**Author details**

Romania

Romania

and Maria Magdalena Duma<sup>5</sup>

Angelica Rita Chiorean1,2\*, Roxana Pintican3

2 Medimages Breast Center, Cluj-Napoca, Romania

5 Micromedica Clinic, Piatra-Neamț, Romania

provided the original work is properly cited.

\*Address all correspondence to: chiorean\_angi@yahoo.com

, Diana Feier1,2, Dan Eniu1,4

1 "Iuliu Hațieganu" University of Medicine and Pharmacy, Cluj-Napoca, Romania

We would like to thank our families for the support and understanding.

3 Department of Radiology and Medical Imaging, County Hospital, Cluj-Napoca,

4 "Prof. Dr. Ion Chiricuță" Oncology Institute, Surgery Department, Cluj-Napoca,

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

**92**

[1] Invasive Lobular Cancer. [Internet]. Available from: http://www. breastcancer.org/symptoms/types/ilc [Accessed: 20 May 2019]

[2] Srivastava S. Breast Malignant, Males, Children [Internet]. 2017. Available from: http://www. pathologyoutlines.com/topic/ breastmalignantlcis.html [Accessed: 20 May 2019]

[3] Jones KN, Magut M, Henrichsen TL, et al. Pure lobular carcinoma of the breast presenting as a hyperechoic mass: Incidence and imaging characteristics. AJR. American Journal of Roentgenology. 2013;**201**:W765-W769. DOI: 10.2214/AJR.12.9742

[4] Breast Cancer Signs and Symptoms online. Available at: https://www.cancer. org/cancer/breast-cancer/about/breastcancer-signs-and-symptoms.html [Accessed: 20 May 2019]

[5] Berg WA, Birdwell RL. Diagnostic Imaging Breast. Salt Lake City: Amyrsis; 2006. pp. 144-147

[6] Selinko VL, Middleton LP, Dempsey PJ. Role of sonography in diagnosing and staging invasive lobular carcinoma. Journal of Clinical Ultrasound. 2004;**32**:323-332. DOI: 10.1002/jcu.20052

[7] Grajo JR, Barr RG. Strain elastography for prediction of breast cancer tumor grades. Journal of Ultrasound in Medicine. 2014;**33**:129-134. DOI: 10.7863/ultra.33.1.129

[8] Olgun DÇ, Korkmazer B, Kılıç F, et al. Use of shear wave elastography to differentiate benign and malignant breast lesions. Diagnostic and Interventional Radiology. 2014;**20**: 239-244. DOI: 10.5152/dir.2014.13306

[9] Chang JM, Won JK, Lee KB, et al. Comparison of shear-wave and

strain ultrasound elastography in the differentiation of benign and malignant breast lesions. AJR. American Journal of Roentgenology. 2013;**201**:347-356. DOI: 10.2214/AJR.12.10416

[10] Sim YT, Vinnicombe S, Whelehan P, Thomson K, Evans A. Value of shear-wave elastography in the diagnosis of symptomatic invasive lobular breast cancer. Clinical Radiology. 2015;**70**:604-609. DOI: 10.1016/j.crad.2015.02.004

[11] Jones KN, Magut M, Henrichsen TL, Boughey JC, Reynolds C, Glazebrook KN. Pure lobular carcinoma of the breast presenting as a hyperechoic mass: Incidence and imaging characteristics. AJR. 2013;**201**:W765-W769. DOI: 10.2214/ AJR.12.9742

[12] Johnson K, Sarma D, Hwang ES. Lobular breast cancer series: Imaging. Breast Cancer Research. 2015;**17**:94. DOI: 10.1186/s13058-015-0605-0

[13] Topps A, Clay V, Absar M, Howe M, Lim Y, Johnson R, et al. The sensitivity of pre-operative axillary staging in breast cancer: Comparison of invasive lobular and ductal carcinoma. European Journal of Surgical Oncology. 2014;**40**:813-817. DOI: 10.1016/j. ejso.2014.03.026

[14] Botticeli A, Mazzotti E, Di Stefano D, et al. Positive impact of elastography in breast cancer diagnosis: An institutional experience. Journal of Ultrasound. 2015;**18**:321-327. DOI: 10.1007/s40477-015-0177-y

[15] Chiorean A, Szep M, Feier D, et al. Impact of strain Elastography on BI-RADS classification in small invasive lobular carcinoma. Medical Ultrasonography. 2018;**20**:148-153. DOI: 10.11152/mu-1272

[16] Boetes C, Veltman J, van Die L, et al. The role of MRI in invasive lobular carcinoma. Breast Cancer Research and Treatment. 2004;**86**:31-37. DOI: 10.1023/B:BREA.0000032921.10481.dc

Chapter 8

Abstract

Shearwave Elastography in

Differentiating Benign and

Binafsha Manzoor Syed, Jawaid Naeem Qureshi

potential in predicting response of neoadjuvant chemotherapy.

Keywords: breast shearwave elastography, scoring system, breast radiology,

All the tissues of the body have some elasticity due to presence of variable amount of elastic tissue. Pathological insult of the tissues causes change in tissue architecture by disturbing elastic tissue proportion. These pathological insults invariably include chronic inflammatory conditions and cancers as well. Thus the physical examination of the body to make idea of the tissue architecture was the fundamental part of the diagnosis making from the ancient period. Palpation was the sole method of diagnosis in ancient period dates back to more than 5000 years ago during the era of Pharaoh. With advancements in technology, different modes of assessment have been introduced in clinical practice notably imaging techniques. Ultrasound and X-rays are the most commonly used economical, non-invasive and highly reliable techniques in clinical practice. Measurement of the stiffness is quite

Shearwave elastography is a new advance technique of the ultrasound with ultrafast shearwave mode which displays evaluation of the elasticity in real time. As the disease process tend to affect stiffness of the tissue thereby distorting its architecture. This architectural change makes the basic principal of the palpation part of the clinical examination. The shearwave elastography uses the principal of palpation. The output of shearwave is displayed in qualitative mode in the form of color change (ranging from blue to red) and quantitative mode as measure of elasticity in kilopascals (ranging from 0 to 300). The soft tissues are penetrated easily giving a homogenous pattern with blue to green color while cancers show color from red to dark red portraying high elasticity. The scoring system for interpretation of the shearwave results suggest that benign lesions show less (i.e., <200 kPa) elasticity while cancers reach high levels (upto 300 kPa). Shearwave elastography has shown superiority as compared to B-mode ultrasound and mammogram in determining the nature of the breast lesions. It has shown high sensitivity in BIRAD 3 and 4 lesions to downgrade and helps in making accurate diagnosis. It has also shown

Malignant Breast Lesions

and Bikha Ram Devrajani

ultrasound, breast cancer imaging

1. Introduction

95

#### Chapter 8

*Ultrasound Elastography*

[16] Boetes C, Veltman J, van Die L, et al. The role of MRI in invasive lobular carcinoma. Breast Cancer Research and Treatment. 2004;**86**:31-37. DOI: 10.1023/B:BREA.0000032921.10481.dc

**94**

## Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions

Binafsha Manzoor Syed, Jawaid Naeem Qureshi and Bikha Ram Devrajani

#### Abstract

Shearwave elastography is a new advance technique of the ultrasound with ultrafast shearwave mode which displays evaluation of the elasticity in real time. As the disease process tend to affect stiffness of the tissue thereby distorting its architecture. This architectural change makes the basic principal of the palpation part of the clinical examination. The shearwave elastography uses the principal of palpation. The output of shearwave is displayed in qualitative mode in the form of color change (ranging from blue to red) and quantitative mode as measure of elasticity in kilopascals (ranging from 0 to 300). The soft tissues are penetrated easily giving a homogenous pattern with blue to green color while cancers show color from red to dark red portraying high elasticity. The scoring system for interpretation of the shearwave results suggest that benign lesions show less (i.e., <200 kPa) elasticity while cancers reach high levels (upto 300 kPa). Shearwave elastography has shown superiority as compared to B-mode ultrasound and mammogram in determining the nature of the breast lesions. It has shown high sensitivity in BIRAD 3 and 4 lesions to downgrade and helps in making accurate diagnosis. It has also shown potential in predicting response of neoadjuvant chemotherapy.

Keywords: breast shearwave elastography, scoring system, breast radiology, ultrasound, breast cancer imaging

#### 1. Introduction

All the tissues of the body have some elasticity due to presence of variable amount of elastic tissue. Pathological insult of the tissues causes change in tissue architecture by disturbing elastic tissue proportion. These pathological insults invariably include chronic inflammatory conditions and cancers as well. Thus the physical examination of the body to make idea of the tissue architecture was the fundamental part of the diagnosis making from the ancient period. Palpation was the sole method of diagnosis in ancient period dates back to more than 5000 years ago during the era of Pharaoh. With advancements in technology, different modes of assessment have been introduced in clinical practice notably imaging techniques. Ultrasound and X-rays are the most commonly used economical, non-invasive and highly reliable techniques in clinical practice. Measurement of the stiffness is quite

old method, the same principal was followed by elastography which measures tissue stiffness and displays it in the output window. Initially strain elastography was introduced where tissue was displaced by applying pressure on tissue by using probe [1].

Shearwave elastography (SWE) is a relatively new (i.e., 2003) advancement of the ultrasound system which uses ultrafast shearwaves for assessment of elasticity of the tissue by using acoustic radiation force excitation and displays in real time [2]. Shearwave elastography has been used in combination with B-mode ultrasound in order to enhance its diagnostic accuracy. A number of studies have been conducted till date showing role of elastography notably assessment of liver fibrosis in chronic hepatitis patients, assessment of thyroid and breast lesions. In all organs it has shown its superiority than conventional B-mode ultrasound in determining the nature of the lesions. In breast diseases it has been studied for its role not only in differentiating benign and malignant lesions, but also investigated in predicting response to neoadjuvant chemotherapy in locally advanced breast cancers. The diagnostic significance of SWE has been studied since its introduction in clinical practice; nevertheless many aspects are still under investigation. In addition, most of the research works done till date has investigated its role in diagnostics; however its role in screening has not been studied yet. This book chapters looks at the basic mechanism of the shearwave elastography, technique of using shearwave elastography in breast, its clinical application in differentiating benign and malignant breast lesions.

#### 2. Mechanism/physics of shearwave elastography

Shearwaves are ultrafast mechanical waves whose propagation is measured while it passes through tissues. The movement of the waves is influenced by the stiffness of the concerned tissue. The mechanism of the shearwaves follows Young's modulus, which has capability to assess difference in the characteristics of different biological tissues and secondly it quantitatively presents tissue stiffness [1]. This reproduction of the stiffness corresponds the palpation of the tissue on clinical examination.

the cancers tend to be harder than the normal tissue and the benign lesions (Figures 1 and 2). Although it is not applicable in all situations as some benign conditions show harder consistency such as a cyst and some cancers show soft consistency like mucinous type. The study conducted on normal tissue showing the soft consistency with averagely blue color on qualitative assessment and normal tissue elasticity of the breast reported to be 30.68 9.11 kPa in the four quadrants while in the nipple areola it was 31.35 kPa [3]. The stiffness shows negative relationship with the age of the patients. As the age advances in particular older women the breast parenchyma is largely replaced by fat. Fat is naturally much softer than the breast parenchyma thus understandably elasticity reduces. In contrast younger patients have more breast parenchyma and firmer breast thus relatively higher

Qualitative appearance of normal breast tissue and benign cyst on shearwave elastography.

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions

DOI: http://dx.doi.org/10.5772/intechopen.87244

A linear array probe with maximum frequency of 12–14 MHz is used for breast elastography (Figure 3). Technique of applying SWE is crucial. The application of probe for SWE is just to place it on the skin, no additional pressure is required. In the experience of the author if pressure is applied on breast tissues it causes false positive results. Thus just placing the probe and holding it perpendicular to the skin

elasticity, though within limits of the normal range.

Invasive ductal carcinoma breast appearance on shearwave elastography.

Figure 1.

Figure 2.

97

4. Breast shearwave probe and technique

The shearwave elastography is based on two mechanisms including a Mach cone, where different spherical waves in single plane make a Mach cone which allows propagation and rebuilding map of Young's modulus. Secondly the ultrafast mode allows up to 5000–30,000 frames per second depending on the nature of the tissue. In situations of smooth propagation of the waves the real time image generated tends to be clear and homogenous while the areas of stiff tissues show disturbances in the traveling and show high intensity colors with heterogeneous echo pattern. In the areas of extreme hardness the waves do not propagate at all resulting in back area known as signal void area or punched out lesions. The technique is implanted in Aixplorer (Supersonic Imagine, Aix-en-Province, France) equipment [1]. The equipment has wide acceptance for assessment of liver fibrosis stage in chronic hepatitis patients where this has largely replaced biopsy. However, for breast tissue it has not yet achieved due popularity among clinicians.

#### 3. Elasticity differences of normal and pathological breast tissues

As the normal understanding the elasticity of the tissue varies with the disease progression. The particular diseases like chronic inflammation and cancers have higher tendency to show higher level of stiffness. It is also a general concept that

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions DOI: http://dx.doi.org/10.5772/intechopen.87244

#### Figure 1.

old method, the same principal was followed by elastography which measures tissue stiffness and displays it in the output window. Initially strain elastography was introduced where tissue was displaced by applying pressure on tissue by using

Shearwave elastography (SWE) is a relatively new (i.e., 2003) advancement of the ultrasound system which uses ultrafast shearwaves for assessment of elasticity of the tissue by using acoustic radiation force excitation and displays in real time [2]. Shearwave elastography has been used in combination with B-mode ultrasound

conducted till date showing role of elastography notably assessment of liver fibrosis in chronic hepatitis patients, assessment of thyroid and breast lesions. In all organs it has shown its superiority than conventional B-mode ultrasound in determining the nature of the lesions. In breast diseases it has been studied for its role not only in differentiating benign and malignant lesions, but also investigated in predicting response to neoadjuvant chemotherapy in locally advanced breast cancers. The diagnostic significance of SWE has been studied since its introduction in clinical practice; nevertheless many aspects are still under investigation. In addition, most of the research works done till date has investigated its role in diagnostics; however its role in screening has not been studied yet. This book chapters looks at the basic

in order to enhance its diagnostic accuracy. A number of studies have been

mechanism of the shearwave elastography, technique of using shearwave

2. Mechanism/physics of shearwave elastography

elastography in breast, its clinical application in differentiating benign and malig-

Shearwaves are ultrafast mechanical waves whose propagation is measured while it passes through tissues. The movement of the waves is influenced by the stiffness of the concerned tissue. The mechanism of the shearwaves follows Young's modulus, which has capability to assess difference in the characteristics of different biological tissues and secondly it quantitatively presents tissue stiffness [1]. This reproduction of the stiffness corresponds the palpation of the tissue on clinical

The shearwave elastography is based on two mechanisms including a Mach cone, where different spherical waves in single plane make a Mach cone which allows propagation and rebuilding map of Young's modulus. Secondly the ultrafast mode allows up to 5000–30,000 frames per second depending on the nature of the tissue. In situations of smooth propagation of the waves the real time image generated tends to be clear and homogenous while the areas of stiff tissues show disturbances in the traveling and show high intensity colors with heterogeneous echo pattern. In the areas of extreme hardness the waves do not propagate at all resulting in back area known as signal void area or punched out lesions. The technique is implanted in Aixplorer (Supersonic Imagine, Aix-en-Province, France) equipment [1]. The equipment has wide acceptance for assessment of liver fibrosis stage in chronic hepatitis patients where this has largely replaced biopsy. However, for

breast tissue it has not yet achieved due popularity among clinicians.

3. Elasticity differences of normal and pathological breast tissues

As the normal understanding the elasticity of the tissue varies with the disease progression. The particular diseases like chronic inflammation and cancers have higher tendency to show higher level of stiffness. It is also a general concept that

probe [1].

Ultrasound Elastography

nant breast lesions.

examination.

96

Qualitative appearance of normal breast tissue and benign cyst on shearwave elastography.

the cancers tend to be harder than the normal tissue and the benign lesions (Figures 1 and 2). Although it is not applicable in all situations as some benign conditions show harder consistency such as a cyst and some cancers show soft consistency like mucinous type. The study conducted on normal tissue showing the soft consistency with averagely blue color on qualitative assessment and normal tissue elasticity of the breast reported to be 30.68 9.11 kPa in the four quadrants while in the nipple areola it was 31.35 kPa [3]. The stiffness shows negative relationship with the age of the patients. As the age advances in particular older women the breast parenchyma is largely replaced by fat. Fat is naturally much softer than the breast parenchyma thus understandably elasticity reduces. In contrast younger patients have more breast parenchyma and firmer breast thus relatively higher elasticity, though within limits of the normal range.

#### 4. Breast shearwave probe and technique

A linear array probe with maximum frequency of 12–14 MHz is used for breast elastography (Figure 3). Technique of applying SWE is crucial. The application of probe for SWE is just to place it on the skin, no additional pressure is required. In the experience of the author if pressure is applied on breast tissues it causes false positive results. Thus just placing the probe and holding it perpendicular to the skin

#### Ultrasound Elastography

There were studies available to suggest that SWE stiffness of the breast cancer has been linked with prediction of the poor survival [9, 10]. The harder the tumor, the poorer the survival. This can be biologically explained by having hard aggressive tumors with high grades and solid consistency resulting in poor survival [11]. A

> Sample size

Conclusion

significant difference in elasticity on SWE. Application of SWE reduces the rate of false positives by 25% in general while for BIRAD category four false negative rate was reduced by 54%

SWE significantly enhance diagnostic accuracy even in smaller tumors (≤2 cm)

mode Ultrasound and SWE. 90% were downgraded by SWE

and SWE and compared with histopathology. SWE was superior in making diagnosis on BIRAD 3 and 4 category

without SWE. The addition of SWE improved specificity from 17 to 98%

sensitivity and specificity in BIRAD 3 and 4 lesions

Addition of SWE increases sensitivity and specificity of diagnosis and differentiating benign and malignant non palpable breast lesions

accuracy in BIRAD 4 category

addition of SWE increases the chance of accurate diagnosis in BIRAD 3 and 4 category

performance of B-mode US, potentially reducing unnecessary biopsies

DCIS was detected within the fibroadenoma

ultrasound

differentiation of the tumors better

peri-tumoral rim on SWE in addition to the grayscale measurement make better comparability with the pathological size of the cancer

2019 396 Malignant and benign breast lesions show

2019 428 Combined approach with B-mode ultrasound and

2019 458 BIRAD category four lesions were evaluated on B-

2018 2273 Multi-center study compared B-mode ultrasound

2017 126 Addition of SWE to conventional B-mode increases

2016 116 Non palpable breast lesions were evaluated.

2015 140 Complex cystic and solid masses showed that

2014 79 Addition of SE or SWE improved the diagnostic

2014 167 Shearwave elastography improves outcome of

2014 86 In smaller tumors ≤15 cm in size addition of the

Clinical Imaging 2018 209 Breast lesions were compared on B-mode with and

Medicine 2015 177 Addition of SWE to B-mode increases diagnostic

Radiology 2014 159 Shearwave increases sensitivity and specificity of US

Radiology 2014 137 Addition of shearwave with stiff rim setting makes

2014 64 Excellent reproducibility

2014 1 (a case report)

S. No Author Name of

1 Doria [12]

2 Choi [13]

3 Zhang [14]

4 Lin [15]

5 Song [9]

6 Wang [16]

7 Choi [17]

8 Kim [18]

9 Lee [19]

10 Youk [20]

11 Kilic [21]

12 Lee [22]

13 Klotz [23]

14 Zhou [24]

15 Park [25]

16 Mullen [26]

99

journal

DOI: http://dx.doi.org/10.5772/intechopen.87244

European Journal of Radiology

British Journal of Radiology

Breast Cancer Research and Treatment

Cancer Management Research

Ultrasound in Medicine and Biology

> European Radiology

> European Journal of Radiology

Ultrasound in Medicine and Biology

Journal of Breast Cancer

Diagnostic and Interventional Imaging

Ultrasound in Medicine and Biology

> Clinical Radiology

Year of publication

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions

Figure 3. Linear-array probe used for breast shearwave elastography.

Figure 4. Clockwise fashion of assessing breast by shearwave elastography.

is just appropriate. However, in deep seated lesions minimal compression may be applied without putting unnecessary pressure on the tumor.

The first stage and important stage is to get good quality homogenous B-mode images. The B-mode provides basis for generation of the SWE. Placing the probe parallel to the duct then moving it in clock wise fashion in all quadrants of the breast allows superficial assessment of whole breast (Figure 4). This is the general screening. In case if there is any lesion visible then detailed examination of the lesion is to be done in addition to the general assessment. The initial qualitative assessment is done followed by application of ROI for measurement of the elasticity.

#### 5. Reliability of SWE as imaging modality in breast

#### 5.1 SWE differentiating benign and malignant breast lesions

Since SWE was brought in clinical practice a number of studies have been conducted on its reliability and compared it with the conventional modes of imaging including ultrasound and mammograms. In addition to individual studies a number of meta-analysis has also been done [4–6]. Invariably all the studies showed superiority of SWE over ultrasound and mammograms alone in particular BIRAD 3 and 4 cases. However, SWE did not differentiate among molecular classes of breast cancer, though higher grades were associated with high elasticity [7]. Another study compared ultrasound and combined ultrasound with SWE to differentiate mastitis and malignancy. With addition of SWE specificity was increased from 11.5 to 96% [8].

There were studies available to suggest that SWE stiffness of the breast cancer has been linked with prediction of the poor survival [9, 10]. The harder the tumor, the poorer the survival. This can be biologically explained by having hard aggressive tumors with high grades and solid consistency resulting in poor survival [11]. A


is just appropriate. However, in deep seated lesions minimal compression may be

allows superficial assessment of whole breast (Figure 4). This is the general screening. In case if there is any lesion visible then detailed examination of the lesion is to be done in addition to the general assessment. The initial qualitative assessment is done followed by application of ROI for measurement of the elasticity.

Since SWE was brought in clinical practice a number of studies have been conducted on its reliability and compared it with the conventional modes of imaging including ultrasound and mammograms. In addition to individual studies a number of meta-analysis has also been done [4–6]. Invariably all the studies showed superiority of SWE over ultrasound and mammograms alone in particular BIRAD 3 and 4 cases. However, SWE did not differentiate among molecular classes of breast cancer, though higher grades were associated with high elasticity [7]. Another study compared ultrasound and combined ultrasound with SWE to differentiate mastitis and malignancy. With addition of SWE specificity was increased from 11.5 to 96% [8].

The first stage and important stage is to get good quality homogenous B-mode images. The B-mode provides basis for generation of the SWE. Placing the probe parallel to the duct then moving it in clock wise fashion in all quadrants of the breast

applied without putting unnecessary pressure on the tumor.

Clockwise fashion of assessing breast by shearwave elastography.

Linear-array probe used for breast shearwave elastography.

Figure 3.

Ultrasound Elastography

Figure 4.

98

5. Reliability of SWE as imaging modality in breast

5.1 SWE differentiating benign and malignant breast lesions


#### Table 1.

Summary of the studies evaluating role of shearwave elastography in differentiating benign and malignant lesions of the breast.

summary of the studies reporting on role of SWE in differentiating benign and malignant lesions is given in Table 1.

#### 5.2 SWE predicting response to neo-adjuvant chemotherapy in locally advanced breast cancer

Shearwave elastography was evaluated to assess its potential role in predicting response to chemotherapy in a number of studies (Table 2). Each tumor has cellular component and the tumor stroma. When there is compact cellular component the tumor tend to show hardness which appears as high elasticity on SWE. While with the action of the chemotherapy; cells start to die and there comes softness which appears as reduction in elasticity of the tumors. Those tumors show response to chemotherapy present with reduced stiffness earlier in the course of treatment (Table 2). Thus invariably all the studies showed that those tumor showing pathological complete response have also shown reduction in the elasticity on SWE earlier [33].

6. Reporting of breast SWE

Figure 5.

101

elastography.

The probe needs to be placed very gently on the breast without application of any pressure. For breast evaluation clockwise 12 measurements have to be taken. The reporting is to be done by using qualitative as well as quantitative findings of the breast tissue including color of the tissue and maximum elasticity values (Figure 5a and b). If there is any additional finding such as signal void area then it has to be described along with its location in the breast. The ROI is placed in all the areas with maximum elasticity level are to be taken into account. The size of the ROI is to be adjusted according to the size of the tumor and the proportion of the heterogeneous tissue including hard and soft parts. The cancers show more heterogeneity then the benign lesions. Thus the highest elasticity is taken as well as reading from heterogenous area to take the ratio of the low elasticity and high elasticity. The breast areas are to be reported followed by the detailed report of the lesion. The specific area report should

Qualitative parameter (a) and quantitative parameters (b) of breast lesion assessment on shearwave

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions

DOI: http://dx.doi.org/10.5772/intechopen.87244

Shearwaves are ultra-fast waves generated by acoustic force radiation travel transversely into the tissues and display output in qualitative and quantitative mode. The qualitative outcome is displayed in the form of color change that ranges from dark blue (i.e., normal tissue) to yellow, orange (i.e., benign) and finally red and dark red (i.e., malignancy) (Figures 5a, 6–9). The corresponding quantitative measurement ranges from 0 to 300 (Figure 5b). The tissue elasticity of the breast

include color, elasticity and the presence of signal void area.

7. Interpretation of shearwave elastography


#### Table 2.

Summary of the studies showing role of shearwave elastography in predicting response to neoadjuvant chemotherapy in locally advanced breast cancer.

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions DOI: http://dx.doi.org/10.5772/intechopen.87244

Figure 5. Qualitative parameter (a) and quantitative parameters (b) of breast lesion assessment on shearwave elastography.

#### 6. Reporting of breast SWE

summary of the studies reporting on role of SWE in differentiating benign and

Summary of the studies evaluating role of shearwave elastography in differentiating benign and malignant

Sample size

Conclusion

information

and stiffness

Conclusion

pathological complete response, which was assessed by reduction in elasticity of the cancer on SWE

Xenograph mouse models were used. Results showed reduced elasticity of the tumors achieving clinical benefit. This reduction was picked up by SWE

chemotherapy and results showed that the tumors achieving clinical benefit showed reduction in the elasticity with 2 cycles

Xenograph mouse models were used. The SWE evaluation showed significant reduction in tumor stiffness after chemotherapy

the elasticity while the areas of higher stiffness were corresponding areas with the residual tumors

2018 80 Out of 80 patients 26% achieved

2016 62 After 2 cycles of neoadjuvant

2015 71 The response areas showed reduction in

2014 115 Provides additional valuable quantitative

2014 116 Shearwave elastography correlated with the grade

Shearwave elastography was evaluated to assess its potential role in predicting response to chemotherapy in a number of studies (Table 2). Each tumor has cellular component and the tumor stroma. When there is compact cellular component the tumor tend to show hardness which appears as high elasticity on SWE. While with the action of the chemotherapy; cells start to die and there comes softness which appears as reduction in elasticity of the tumors. Those tumors show response to chemotherapy present with reduced stiffness earlier in the course of treatment (Table 2). Thus invariably all the studies showed that those tumor showing pathological complete

5.2 SWE predicting response to neo-adjuvant chemotherapy in locally

response have also shown reduction in the elasticity on SWE earlier [33].

Year of publication Sample size

model

2018 Mouse

2016 Mouse

Summary of the studies showing role of shearwave elastography in predicting response to neoadjuvant

model

malignant lesions is given in Table 1.

advanced breast cancer

S. No Author Name of

1 Evan [28] Clinical

2 Wang [29] British

3 Jing [30] Journal of

5 Lee[32] Annals of

chemotherapy in locally advanced breast cancer.

4 Chamming's [31]

Table 2.

100

journal

Radiology

Journal of Radiology

Ultrasound in Medicine

Ultrasound in Medicine and Biology

Surgical Oncology

S. No Author Name of

Ultrasound Elastography

17 Cebi Olgun [27]

18 Choi [11]

lesions of the breast.

Table 1.

journal

Diagnostic and Interventional Imaging

Ultrasound in Medicine and Biology

Year of publication

> The probe needs to be placed very gently on the breast without application of any pressure. For breast evaluation clockwise 12 measurements have to be taken. The reporting is to be done by using qualitative as well as quantitative findings of the breast tissue including color of the tissue and maximum elasticity values (Figure 5a and b). If there is any additional finding such as signal void area then it has to be described along with its location in the breast. The ROI is placed in all the areas with maximum elasticity level are to be taken into account. The size of the ROI is to be adjusted according to the size of the tumor and the proportion of the heterogeneous tissue including hard and soft parts. The cancers show more heterogeneity then the benign lesions. Thus the highest elasticity is taken as well as reading from heterogenous area to take the ratio of the low elasticity and high elasticity. The breast areas are to be reported followed by the detailed report of the lesion. The specific area report should include color, elasticity and the presence of signal void area.

#### 7. Interpretation of shearwave elastography

Shearwaves are ultra-fast waves generated by acoustic force radiation travel transversely into the tissues and display output in qualitative and quantitative mode. The qualitative outcome is displayed in the form of color change that ranges from dark blue (i.e., normal tissue) to yellow, orange (i.e., benign) and finally red and dark red (i.e., malignancy) (Figures 5a, 6–9). The corresponding quantitative measurement ranges from 0 to 300 (Figure 5b). The tissue elasticity of the breast

Figure 6. Benign breast cyst on shearwave elastography.

As the elasticity increases the kilopascal measurements also rises. However, in certain situations where intrinsic factors of the tumor show false negative results such as in situ cancers. While age of the patients, high risk lesions, tumors closer to the chest wall or overlying skin or deep seated tumors were likely to develop false positives results [13]. The study including 428 smaller tumor (≤2 cm) compared conventional B-mode ultrasound with SWE combined approach. The results showed that SWE combined approach was superior than B-mode alone, however in situ cancers showed false negative results [13]. Another study showed that presence of in situ tumor, calcifications and tumors near the nipple are likely to produce inaccurate results [34]. The study was conducted on non-palpable breast lesions including 79 malignant and 73 benign breast lesions. The smaller size of the lesion was also associated with inaccurate results in the study [34]. The inaccuracies in SWE interpretation could be explained by the nature of the lesion such as the case of in situ cancers, which has not yet produced that high reaction of the surrounding peri-tumoral tissue. The age of the patient and the location of the tumor potentially have influence of the breast tissue elasticity. The study including 1137 tumors to differentiate characteristics of the types of breast cancers on SWE. There was no characteristic difference in different histological types of cancers with exception of tubular type which showed less elasticity [35]. The fibroadenomas on the other hand show false positive expression if they were larger in size [36]. Interestingly lobular carcinoma has potential to display itself as benign or probably benign on B-mode ultrasound or mammogram but SWE showed higher rate of picking up lobular cancers [37]. The characteristics of the benign and malignant lesions were evaluated in a prospective cross-sectional study including 119 women. These patients underwent clinical breast examination, followed by conventional ultrasound then SWE and finally ultrasound guided tissue biopsy. The results showed that the benign lesions tend to be oval or round in shape with homogenous echopattern. Their color ranges from blue to yellow and green but reasonably homogenous with low elasticity. On the other hand malignant lesions were in contrast with irregular margins, heterogeneous echopattern and color from red to dark red in correlation with high elasticity [38]. The debatable issue lies with SWE is the operator dependency which is attached

Invasive ductal carcinoma appearance on shearwave elastography—without signal void area.

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions

DOI: http://dx.doi.org/10.5772/intechopen.87244

to B-mode ultrasound by default. The application of the probe is crucial with dependency on the operator; however there is less influence on the results if the

In this regard, a study compared an operator with 15 years experience with that having 1 year [39]. The reproducibility of the results was high with SWE showing

technique of the probe application is correct.

103

Figure 9.

#### Figure 7.

Invasive lobular carcinoma appearance on shearwave elastography.

Figure 8. Invasive ductal carcinoma appearance with signal void area on shearwave elastography.

showed negative correlation with the age i.e., as the age advances the tissue elasticity reduces [3]. This can be explained by natural evolution of the breast where with advancing age breast parenchyma replaced by fat tissue. This should always be borne in mind that high resolution good quality images can only be interpreted. In case if there is so much of background noise and the images are not giving a clear description it's better to avoid interpretation of such images. In this regard the best approach is to do a combine approach with B-mode first. With the B-mode imaging identify the lesion and its characteristics then SWE be applied on the lesion in order to avoid influence of artifacts.

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions DOI: http://dx.doi.org/10.5772/intechopen.87244

Figure 9. Invasive ductal carcinoma appearance on shearwave elastography—without signal void area.

As the elasticity increases the kilopascal measurements also rises. However, in certain situations where intrinsic factors of the tumor show false negative results such as in situ cancers. While age of the patients, high risk lesions, tumors closer to the chest wall or overlying skin or deep seated tumors were likely to develop false positives results [13]. The study including 428 smaller tumor (≤2 cm) compared conventional B-mode ultrasound with SWE combined approach. The results showed that SWE combined approach was superior than B-mode alone, however in situ cancers showed false negative results [13]. Another study showed that presence of in situ tumor, calcifications and tumors near the nipple are likely to produce inaccurate results [34]. The study was conducted on non-palpable breast lesions including 79 malignant and 73 benign breast lesions. The smaller size of the lesion was also associated with inaccurate results in the study [34]. The inaccuracies in SWE interpretation could be explained by the nature of the lesion such as the case of in situ cancers, which has not yet produced that high reaction of the surrounding peri-tumoral tissue. The age of the patient and the location of the tumor potentially have influence of the breast tissue elasticity. The study including 1137 tumors to differentiate characteristics of the types of breast cancers on SWE. There was no characteristic difference in different histological types of cancers with exception of tubular type which showed less elasticity [35]. The fibroadenomas on the other hand show false positive expression if they were larger in size [36]. Interestingly lobular carcinoma has potential to display itself as benign or probably benign on B-mode ultrasound or mammogram but SWE showed higher rate of picking up lobular cancers [37].

The characteristics of the benign and malignant lesions were evaluated in a prospective cross-sectional study including 119 women. These patients underwent clinical breast examination, followed by conventional ultrasound then SWE and finally ultrasound guided tissue biopsy. The results showed that the benign lesions tend to be oval or round in shape with homogenous echopattern. Their color ranges from blue to yellow and green but reasonably homogenous with low elasticity. On the other hand malignant lesions were in contrast with irregular margins, heterogeneous echopattern and color from red to dark red in correlation with high elasticity [38].

The debatable issue lies with SWE is the operator dependency which is attached to B-mode ultrasound by default. The application of the probe is crucial with dependency on the operator; however there is less influence on the results if the technique of the probe application is correct.

In this regard, a study compared an operator with 15 years experience with that having 1 year [39]. The reproducibility of the results was high with SWE showing

showed negative correlation with the age i.e., as the age advances the tissue elasticity reduces [3]. This can be explained by natural evolution of the breast where with advancing age breast parenchyma replaced by fat tissue. This should always be borne in mind that high resolution good quality images can only be interpreted. In case if there is so much of background noise and the images are not giving a clear description it's better to avoid interpretation of such images. In this regard the best approach is to do a combine approach with B-mode first. With the B-mode imaging identify the lesion and its characteristics then SWE be applied on the lesion in order

Invasive ductal carcinoma appearance with signal void area on shearwave elastography.

to avoid influence of artifacts.

Figure 6.

Ultrasound Elastography

Figure 7.

Figure 8.

102

Benign breast cyst on shearwave elastography.

Invasive lobular carcinoma appearance on shearwave elastography.

#### Ultrasound Elastography

less dependency on operator experience for interpretation, while intra-observer reproducibility has been reported to be 0.789 on SWE [25].

There are a number of parameters which could be utilized for interpretation such as mean elasticity value, minimum elasticity value and maximum elasticity. Most of the studies showed maximum elasticity value in kilopascals as the most reliable to be considered. However, all parameters need to be observed in cases of highly heterogeneous cancers.

#### 8. Breast lesion scoring system

The authors have developed a scoring system for better diagnostic yield of shearwave elastography by combining qualitative and quantitative characteristics of the breast lesions. The scoring system takes into account the change of color, quantitative measurement of stiffness in kilopascals (kPa) and presence or absence of the signal void area (i.e., punched out lesion). A summary of the scoring system is given in Table 3.

Hard solid tumors showed dark color on qualitative measure, while benign soft tumors show natural color including blue, yellow orange. Normal breast tissue is blue in color. Fibrocystic lesion change color from blue to yellow or even orange but none of the benign lesions turn dark red. Similarly all the malignant lesion were red in different shades. Quantitative measurement of the kPa of benign lesions was low with less stiffness while solid tumor and cancers show score >200. Dark red color on qualitative scale and >250 kPa was invariably seen in cancers. When the cancer gets really hard and shear waves fail to penetrate resulting in signal void area punched out lesion. There was an exception of breast abscess which also showed signal void area due to cavity. The differing point of the breast abscess and the malignant breast lesion was based on color and mean kPa score while signal void area was seen in majority of both cases. Figures 10–12 portray the breast lesion from benign to malignant pathologies.


9. Conclusion

Figure 12.

105

Figure 11.

Fibrocystic disease on shearwave elastography.

DOI: http://dx.doi.org/10.5772/intechopen.87244

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions

successfully avoiding negative biopsies.

Invasive ductal carcinoma of breast on shearwave elastography.

Shearwave elastography is a new advanced technique with ultrafast mode of shearwaves to assess elasticity of the tissue. It has established role in assessment of the liver fibrosis. The available literature favors use of shearwave elastography in combination with B-mode ultrasound to enhance diagnostic accuracy of the conventional ultrasound. However, it has not been widely used in clinical practice. Though it has shown great potential in differentiating BIRAD 3 and 4 categories and

#### Table 3.

Scoring system to interpret Shearwave elastography findings of breast lesions.

Figure 10. Benign breast disease on shearwave elastography.

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions DOI: http://dx.doi.org/10.5772/intechopen.87244

Figure 11. Fibrocystic disease on shearwave elastography.

less dependency on operator experience for interpretation, while intra-observer

The authors have developed a scoring system for better diagnostic yield of shearwave elastography by combining qualitative and quantitative characteristics of the breast lesions. The scoring system takes into account the change of color, quantitative measurement of stiffness in kilopascals (kPa) and presence or absence of the signal void area (i.e., punched out lesion). A summary of the scoring system is given in Table 3. Hard solid tumors showed dark color on qualitative measure, while benign soft tumors show natural color including blue, yellow orange. Normal breast tissue is blue in color. Fibrocystic lesion change color from blue to yellow or even orange but none of the benign lesions turn dark red. Similarly all the malignant lesion were red in different shades. Quantitative measurement of the kPa of benign lesions was low with less stiffness while solid tumor and cancers show score >200. Dark red color on qualitative scale and >250 kPa was invariably seen in cancers. When the cancer gets really hard and shear waves fail to penetrate resulting in signal void area punched out lesion. There was an exception of breast abscess which also showed signal void area due to cavity. The differing point of the breast abscess and the malignant breast lesion was based on color and mean kPa score while signal void area was seen in majority of both cases. Figures 10–12 portray the breast lesion from benign to

Parameter Score 1 Score 2 Score 3 Color Blue, yellow, orange Red, dark red Dark red Mean kPa range <200 >200 but <250 >250 Punched out lesion status Absent Present May be present

Scoring system to interpret Shearwave elastography findings of breast lesions.

There are a number of parameters which could be utilized for interpretation such as mean elasticity value, minimum elasticity value and maximum elasticity. Most of the studies showed maximum elasticity value in kilopascals as the most reliable to be considered. However, all parameters need to be observed in cases of

reproducibility has been reported to be 0.789 on SWE [25].

highly heterogeneous cancers.

Ultrasound Elastography

malignant pathologies.

Table 3.

Figure 10.

104

Benign breast disease on shearwave elastography.

8. Breast lesion scoring system

Figure 12. Invasive ductal carcinoma of breast on shearwave elastography.

#### 9. Conclusion

Shearwave elastography is a new advanced technique with ultrafast mode of shearwaves to assess elasticity of the tissue. It has established role in assessment of the liver fibrosis. The available literature favors use of shearwave elastography in combination with B-mode ultrasound to enhance diagnostic accuracy of the conventional ultrasound. However, it has not been widely used in clinical practice. Though it has shown great potential in differentiating BIRAD 3 and 4 categories and successfully avoiding negative biopsies.

Ultrasound Elastography

#### Author details

Binafsha Manzoor Syed<sup>1</sup> \*, Jawaid Naeem Qureshi<sup>2</sup> and Bikha Ram Devrajani<sup>3</sup> References

487-495

Nov 25

[1] Gennisson JL, Deffieux T, Fink M, Tanter M. Ultrasound elastography: Principles and techniques. Diagnostic and Interventional Imaging. 2013;94(5):

DOI: http://dx.doi.org/10.5772/intechopen.87244

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions

shear wave elastography for differential diagnosis between mastitis and breast malignancy. Clinical Hemorheology and Microcirculation. 2018;70(3):347-354

[9] Song EJ, Sohn YM, Seo M. Diagnostic

elastography and B-mode ultrasound to differentiate benign and malignant breast lesions: The emphasis on the cutoff value of qualitative and quantitative parameters. Clinical Imaging. 2018;50:302-307

[10] Evans A, Sim YT, Pourreyron C, Thompson A, Jordan L, Fleming D, et al.

measured by shear wave elastography is independently associated with breast cancer-specific survival. Breast Cancer Research and Treatment. 2018;171(2):

[11] Choi WJ, Kim HH, Cha JH, Shin HJ, Kim H, Chae EY, et al. Predicting prognostic factors of breast cancer using shear wave elastography. Ultrasound in Medicine and Biology. 2014;40(2):

[12] Doria MT, Jales RM, Conz L, Derchain SFM, Sarian LOZ. Diagnostic accuracy of shear wave elastography— Virtual touch™ imaging quantification in the evaluation of breast masses: Impact on ultrasonography's specificity

and its ultimate clinical benefit. European Journal of Radiology. 2019;

[13] Choi HY, Seo M, Sohn YM, Hwang JH, Song EJ, Min SY, et al. Shear wave elastography for the diagnosis of small (≦2 cm) breast lesions: Added value and factors associated with false results. The British Journal of Radiology. 2019;

[14] Zhang Q, Song S, Xiao Y, Chen S, Shi J, Zheng H. Dual-mode artificiallyintelligent diagnosis of breast tumours in shear-wave elastography and B-mode

Pre-operative stromal stiffness

383-389

269-274

113:74-80

92(1097):20180341

performances of shear-wave

[2] Nakashima K, Shiina T, Sakurai M, Enokido K, Endo T, Tsunoda H, et al. JSUM ultrasound elastography practice guidelines: Breast. Journal of Medical Ultrasonics. 2013;40(4):359-391

[3] Sendur HN, Gultekin S, Salimli L, Cindil E, Cerit M, Sendur AB. Determination of normal breast and areolar skin elasticity using shear wave elastography. Journal of Ultrasound in Medicine. Jul 2019;38(7):1815-1822. DOI: 10.1002/jum.14877. Epub 2018

[4] Huang R, Jiang L, Xu Y, Gong Y, Ran H, Wang Z, et al. Comparative diagnostic

ultrasound and shear wave elastography in differentiating benign and malignant lesions: A network meta-analysis. Frontiers in Oncology. 2019;9:102

[5] Luo J, Cao Y, Nian W, Zeng X, Zhang H, Yue Y, et al. Benefit of shear-wave elastography in the differential

diagnosis of breast lesion: A diagnostic

[6] Xue Y, Yao S, Li X, Zhang H. Value

Ultrasonography. 2018;1(1):43-49

[7] Ganau S, Andreu FJ, Escribano F, Martin A, Tortajada L, Villajos M, et al.

immunohistochemical profiles in invasive breast cancer: Evaluation of maximum and mean elasticity values. European Journal of Radiology. 2015;84(4):617-622

[8] Liu SQ, Liu YP, Zhou BG, Deng XH, Li XL, Xiang LH, et al. Two-dimensional

Shear-wave elastography and

107

of shear wave elastography in discriminating malignant and benign breast lesions: A meta-analysis. Medicine. 2017;96(42):e7412

meta-analysis. Medical

accuracy of contrast-enhanced

1 Medical Research Center, Liaquat University of Medical and Health Sciences, Jamshoro, Pakistan

2 Department of Surgery, Indus Medical College, Tando Mohammad Khan, Pakistan

3 Department of Medicine, Liaquat University of Medical and Health Sciences, Jamshoro, Pakistan

\*Address all correspondence to: drbinafsha@hotmail.com

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions DOI: http://dx.doi.org/10.5772/intechopen.87244

#### References

[1] Gennisson JL, Deffieux T, Fink M, Tanter M. Ultrasound elastography: Principles and techniques. Diagnostic and Interventional Imaging. 2013;94(5): 487-495

[2] Nakashima K, Shiina T, Sakurai M, Enokido K, Endo T, Tsunoda H, et al. JSUM ultrasound elastography practice guidelines: Breast. Journal of Medical Ultrasonics. 2013;40(4):359-391

[3] Sendur HN, Gultekin S, Salimli L, Cindil E, Cerit M, Sendur AB. Determination of normal breast and areolar skin elasticity using shear wave elastography. Journal of Ultrasound in Medicine. Jul 2019;38(7):1815-1822. DOI: 10.1002/jum.14877. Epub 2018 Nov 25

[4] Huang R, Jiang L, Xu Y, Gong Y, Ran H, Wang Z, et al. Comparative diagnostic accuracy of contrast-enhanced ultrasound and shear wave elastography in differentiating benign and malignant lesions: A network meta-analysis. Frontiers in Oncology. 2019;9:102

[5] Luo J, Cao Y, Nian W, Zeng X, Zhang H, Yue Y, et al. Benefit of shear-wave elastography in the differential diagnosis of breast lesion: A diagnostic meta-analysis. Medical Ultrasonography. 2018;1(1):43-49

[6] Xue Y, Yao S, Li X, Zhang H. Value of shear wave elastography in discriminating malignant and benign breast lesions: A meta-analysis. Medicine. 2017;96(42):e7412

[7] Ganau S, Andreu FJ, Escribano F, Martin A, Tortajada L, Villajos M, et al. Shear-wave elastography and immunohistochemical profiles in invasive breast cancer: Evaluation of maximum and mean elasticity values. European Journal of Radiology. 2015;84(4):617-622

[8] Liu SQ, Liu YP, Zhou BG, Deng XH, Li XL, Xiang LH, et al. Two-dimensional shear wave elastography for differential diagnosis between mastitis and breast malignancy. Clinical Hemorheology and Microcirculation. 2018;70(3):347-354

[9] Song EJ, Sohn YM, Seo M. Diagnostic performances of shear-wave elastography and B-mode ultrasound to differentiate benign and malignant breast lesions: The emphasis on the cutoff value of qualitative and quantitative parameters. Clinical Imaging. 2018;50:302-307

[10] Evans A, Sim YT, Pourreyron C, Thompson A, Jordan L, Fleming D, et al. Pre-operative stromal stiffness measured by shear wave elastography is independently associated with breast cancer-specific survival. Breast Cancer Research and Treatment. 2018;171(2): 383-389

[11] Choi WJ, Kim HH, Cha JH, Shin HJ, Kim H, Chae EY, et al. Predicting prognostic factors of breast cancer using shear wave elastography. Ultrasound in Medicine and Biology. 2014;40(2): 269-274

[12] Doria MT, Jales RM, Conz L, Derchain SFM, Sarian LOZ. Diagnostic accuracy of shear wave elastography— Virtual touch™ imaging quantification in the evaluation of breast masses: Impact on ultrasonography's specificity and its ultimate clinical benefit. European Journal of Radiology. 2019; 113:74-80

[13] Choi HY, Seo M, Sohn YM, Hwang JH, Song EJ, Min SY, et al. Shear wave elastography for the diagnosis of small (≦2 cm) breast lesions: Added value and factors associated with false results. The British Journal of Radiology. 2019; 92(1097):20180341

[14] Zhang Q, Song S, Xiao Y, Chen S, Shi J, Zheng H. Dual-mode artificiallyintelligent diagnosis of breast tumours in shear-wave elastography and B-mode

Author details

Ultrasound Elastography

Jamshoro, Pakistan

Jamshoro, Pakistan

Pakistan

106

Binafsha Manzoor Syed<sup>1</sup>

\*, Jawaid Naeem Qureshi<sup>2</sup> and Bikha Ram Devrajani<sup>3</sup>

1 Medical Research Center, Liaquat University of Medical and Health Sciences,

3 Department of Medicine, Liaquat University of Medical and Health Sciences,

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

2 Department of Surgery, Indus Medical College, Tando Mohammad Khan,

\*Address all correspondence to: drbinafsha@hotmail.com

provided the original work is properly cited.

ultrasound using deep polynomial networks. Medical Engineering and Physics. 2019;64:1-6

[15] Lin X, Chang C, Wu C, Chen Q, Peng Y, Luo B, et al. Confirmed value of shear wave elastography for ultrasound characterization of breast masses using a conservative approach in Chinese women: A large-size prospective multicenter trial. Cancer Management and Research. 2018;10:4447-4458

[16] Wang M, Yang Z, Liu C, Yan J, Zhang W, Sun J, et al. Differential diagnosis of breast category 3 and 4 nodules through BI-RADS classification in conjunction with shear wave elastography. Ultrasound in Medicine and Biology. 2017;43(3):601-606

[17] Choi JS, Han BK, Ko EY, Ko ES, Shin JH, Kim GR. Additional diagnostic value of shear-wave elastography and color doppler US for evaluation of breast nonmass lesions detected at B-mode US. European Radiology. 2016;26(10): 3542-3549

[18] Kim SJ, Ko KH, Jung HK, Kim H. Shear wave elastography: Is it a valuable additive method to conventional ultrasound for the diagnosis of small (≦2 cm) breast cancer? Medicine. 2015; 94(42):e1540

[19] Lee BE, Chung J, Cha ES, Lee JE, Kim JH. Role of shear-wave elastography (SWE) in complex cystic and solid breast lesions in comparison with conventional ultrasound. European Journal of Radiology. 2015;84(7): 1236-1241

[20] Youk JH, Son EJ, Gweon HM, Kim H, Park YJ, Kim JA. Comparison of strain and shear wave elastography for the differentiation of benign from malignant breast lesions, combined with B-mode ultrasonography: Qualitative and quantitative assessments. Ultrasound in Medicine and Biology. 2014;40(10):2336-2344

[21] Kilic F, Ustabasioglu FE, Samanci C, Bas A, Velidedeoglu M, Kilicaslan T, et al. Ductal carcinoma in situ detected by shear wave elastography within a fibroadenoma. Journal of Breast Cancer. 2014;17(2):180-183

Identification of pathological complete

DOI: http://dx.doi.org/10.5772/intechopen.87244

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions

Factors associated with false negative and false positive results. European Radiology. 2017;27(9):3788-3798

[35] Evans A, Sim YT, Thomson K, Jordan L, Purdie C, Vinnicombe SJ. Shear wave elastography of breast cancer: Sensitivity according to histological type in a large cohort.

Breast. 2016;26:115-118

71(1):92-95

604-609

[36] Elseedawy M, Whelehan P, Vinnicombe S, Thomson K, Evans A. Factors influencing the stiffness of fibroadenomas at shear wave

elastography. Clinical Radiology. 2016;

[37] Sim YT, Vinnicombe S, Whelehan P, Thomson K, Evans A. Value of shearwave elastography in the diagnosis of symptomatic invasive lobular breast cancer. Clinical Radiology. 2015;70(6):

[38] Hari S, Paul SB, Vidyasagar R, Dhamija E, Adarsh AD, Thulkar S, et al. Breast mass characterization using shear wave elastography and ultrasound. Diagnostic and Interventional Imaging.

[39] Aslan H, Pourbagher A, Ozen M. The role of shear-wave elastography in the differentiation of benign and malign non-mass lesions of the breast. Annali Italiani di Chirurgia. 2018;89:385-391

2018;99(11):699-707

[29] Wang JW, Guo ZX, Lin QG, Zheng W, Zhuang SL, Lin SY, et al. Ultrasound elastography as an imaging biomarker for detection of early tumor response to chemotherapy in a murine breast cancer model: A feasibility study. The British Journal of Radiology. 2018;91(1085):

[30] Jing H, Cheng W, Li ZY, Ying L, Wang QC, Wu T, et al. Early evaluation of relative changes in tumor stiffness by shear wave elastography predicts the response to neoadjuvant chemotherapy in patients with breast cancer. Journal of Ultrasound in Medicine. 2016;35(8):

[31] Chamming's F, Le-Frere-Belda MA, Latorre-Ossa H, Fitoussi V, Redheuil A, Assayag F, et al. Supersonic shear wave elastography of response to anti-cancer therapy in a xenograft tumor model. Ultrasound in Medicine and Biology.

[32] Lee SH, Chang JM, Han W, Moon HG, Koo HR, Gweon HM, et al. Shearwave elastography for the detection of residual breast cancer after neoadjuvant chemotherapy. Annals of Surgical Oncology. 2015;22(Suppl 3):S376-S384

[33] Evans A, Whelehan P, Thompson A, Purdie C, Jordan L, Macaskill J, et al. Prediction of pathological complete response to neoadjuvant chemotherapy for primary breast cancer comparing interim ultrasound, shear wave

elastography and MRI. Ultraschall in der

[34] Park SY, Choi JS, Han BK, Ko EY, Ko ES. Shear wave elastography in the diagnosis of breast non-mass lesions:

Medizin. 2018;39(4):422-431

109

response after neoadjuvant chemotherapy for breast cancer: Comparison of greyscale ultrasound, shear wave elastography, and MRI. Clinical Radiology. 2018;73(10):910.

e1-910.e6

20170698

1619-1627

2016;42(4):924-930

[22] Lee SH, Chang JM, Kim WH, Bae MS, Seo M, Koo HR, et al. Added value of shear-wave elastography for evaluation of breast masses detected with screening US imaging. Radiology. 2014;273(1):61-69

[23] Klotz T, Boussion V, Kwiatkowski F, Dieu-de Fraissinette V, Bailly-Glatre A, Lemery S, et al. Shear wave elastography contribution in ultrasound diagnosis management of breast lesions. Diagnostic and Interventional Imaging. 2014;95(9):813-824

[24] Zhou J, Zhan W, Chang C, Zhang X, Jia Y, Dong Y, et al. Breast lesions: Evaluation with shear wave elastography, with special emphasis on the "stiff rim" sign. Radiology. 2014; 272(1):63-72

[25] Park HY, Han KH, Yoon JH, Moon HJ, Kim MJ, Kim EK. Intra-observer reproducibility and diagnostic performance of breast shear-wave elastography in Asian women. Ultrasound in Medicine and Biology. 2014;40(6):1058-1064

[26] Mullen R, Thompson JM, Moussa O, Vinnicombe S, Evans A. Shear-wave elastography contributes to accurate tumour size estimation when assessing small breast cancers. Clinical Radiology. 2014;69(12):1259-1263

[27] Cebi Olgun D, Korkmazer B, Kilic F, Dikici AS, Velidedeoglu M, Aydogan F, et al. Use of shear wave elastography to differentiate benign and malignant breast lesions. Diagnostic and Interventional Radiology. 2014;20(3):239-244

[28] Evans A, Whelehan P, Thompson A, Purdie C, Jordan L, Macaskill J, et al.

Shearwave Elastography in Differentiating Benign and Malignant Breast Lesions DOI: http://dx.doi.org/10.5772/intechopen.87244

Identification of pathological complete response after neoadjuvant chemotherapy for breast cancer: Comparison of greyscale ultrasound, shear wave elastography, and MRI. Clinical Radiology. 2018;73(10):910. e1-910.e6

ultrasound using deep polynomial networks. Medical Engineering and [21] Kilic F, Ustabasioglu FE, Samanci C, Bas A, Velidedeoglu M, Kilicaslan T, et al. Ductal carcinoma in situ detected by shear wave elastography within a fibroadenoma. Journal of Breast Cancer.

[22] Lee SH, Chang JM, Kim WH, Bae MS, Seo M, Koo HR, et al. Added value

[23] Klotz T, Boussion V, Kwiatkowski F, Dieu-de Fraissinette V, Bailly-Glatre A,

elastography contribution in ultrasound diagnosis management of breast lesions. Diagnostic and Interventional Imaging.

[24] Zhou J, Zhan W, Chang C, Zhang X, Jia Y, Dong Y, et al. Breast lesions: Evaluation with shear wave

elastography, with special emphasis on the "stiff rim" sign. Radiology. 2014;

[25] Park HY, Han KH, Yoon JH, Moon HJ, Kim MJ, Kim EK. Intra-observer reproducibility and diagnostic performance of breast shear-wave elastography in Asian women. Ultrasound in Medicine and Biology.

[26] Mullen R, Thompson JM, Moussa O, Vinnicombe S, Evans A. Shear-wave elastography contributes to accurate tumour size estimation when assessing small breast cancers. Clinical Radiology.

[27] Cebi Olgun D, Korkmazer B, Kilic F, Dikici AS, Velidedeoglu M, Aydogan F, et al. Use of shear wave elastography to differentiate benign and malignant breast lesions. Diagnostic and Interventional Radiology. 2014;20(3):239-244

[28] Evans A, Whelehan P, Thompson A, Purdie C, Jordan L, Macaskill J, et al.

of shear-wave elastography for evaluation of breast masses detected with screening US imaging. Radiology.

Lemery S, et al. Shear wave

2014;17(2):180-183

2014;273(1):61-69

2014;95(9):813-824

272(1):63-72

2014;40(6):1058-1064

2014;69(12):1259-1263

[15] Lin X, Chang C, Wu C, Chen Q, Peng Y, Luo B, et al. Confirmed value of shear wave elastography for ultrasound characterization of breast masses using a conservative approach in Chinese women: A large-size prospective multicenter trial. Cancer Management and Research. 2018;10:4447-4458

[16] Wang M, Yang Z, Liu C, Yan J, Zhang W, Sun J, et al. Differential diagnosis of breast category 3 and 4 nodules through BI-RADS classification

in conjunction with shear wave elastography. Ultrasound in Medicine and Biology. 2017;43(3):601-606

3542-3549

94(42):e1540

1236-1241

108

[17] Choi JS, Han BK, Ko EY, Ko ES, Shin JH, Kim GR. Additional diagnostic value of shear-wave elastography and color doppler US for evaluation of breast nonmass lesions detected at B-mode US. European Radiology. 2016;26(10):

[18] Kim SJ, Ko KH, Jung HK, Kim H. Shear wave elastography: Is it a valuable

[19] Lee BE, Chung J, Cha ES, Lee JE,

elastography (SWE) in complex cystic and solid breast lesions in comparison with conventional ultrasound. European Journal of Radiology. 2015;84(7):

[20] Youk JH, Son EJ, Gweon HM, Kim H, Park YJ, Kim JA. Comparison of strain and shear wave elastography for the differentiation of benign from malignant breast lesions, combined with B-mode ultrasonography: Qualitative

and quantitative assessments. Ultrasound in Medicine and Biology.

2014;40(10):2336-2344

Kim JH. Role of shear-wave

additive method to conventional ultrasound for the diagnosis of small (≦2 cm) breast cancer? Medicine. 2015;

Physics. 2019;64:1-6

Ultrasound Elastography

[29] Wang JW, Guo ZX, Lin QG, Zheng W, Zhuang SL, Lin SY, et al. Ultrasound elastography as an imaging biomarker for detection of early tumor response to chemotherapy in a murine breast cancer model: A feasibility study. The British Journal of Radiology. 2018;91(1085): 20170698

[30] Jing H, Cheng W, Li ZY, Ying L, Wang QC, Wu T, et al. Early evaluation of relative changes in tumor stiffness by shear wave elastography predicts the response to neoadjuvant chemotherapy in patients with breast cancer. Journal of Ultrasound in Medicine. 2016;35(8): 1619-1627

[31] Chamming's F, Le-Frere-Belda MA, Latorre-Ossa H, Fitoussi V, Redheuil A, Assayag F, et al. Supersonic shear wave elastography of response to anti-cancer therapy in a xenograft tumor model. Ultrasound in Medicine and Biology. 2016;42(4):924-930

[32] Lee SH, Chang JM, Han W, Moon HG, Koo HR, Gweon HM, et al. Shearwave elastography for the detection of residual breast cancer after neoadjuvant chemotherapy. Annals of Surgical Oncology. 2015;22(Suppl 3):S376-S384

[33] Evans A, Whelehan P, Thompson A, Purdie C, Jordan L, Macaskill J, et al. Prediction of pathological complete response to neoadjuvant chemotherapy for primary breast cancer comparing interim ultrasound, shear wave elastography and MRI. Ultraschall in der Medizin. 2018;39(4):422-431

[34] Park SY, Choi JS, Han BK, Ko EY, Ko ES. Shear wave elastography in the diagnosis of breast non-mass lesions:

Factors associated with false negative and false positive results. European Radiology. 2017;27(9):3788-3798

[35] Evans A, Sim YT, Thomson K, Jordan L, Purdie C, Vinnicombe SJ. Shear wave elastography of breast cancer: Sensitivity according to histological type in a large cohort. Breast. 2016;26:115-118

[36] Elseedawy M, Whelehan P, Vinnicombe S, Thomson K, Evans A. Factors influencing the stiffness of fibroadenomas at shear wave elastography. Clinical Radiology. 2016; 71(1):92-95

[37] Sim YT, Vinnicombe S, Whelehan P, Thomson K, Evans A. Value of shearwave elastography in the diagnosis of symptomatic invasive lobular breast cancer. Clinical Radiology. 2015;70(6): 604-609

[38] Hari S, Paul SB, Vidyasagar R, Dhamija E, Adarsh AD, Thulkar S, et al. Breast mass characterization using shear wave elastography and ultrasound. Diagnostic and Interventional Imaging. 2018;99(11):699-707

[39] Aslan H, Pourbagher A, Ozen M. The role of shear-wave elastography in the differentiation of benign and malign non-mass lesions of the breast. Annali Italiani di Chirurgia. 2018;89:385-391

**111**

Section 3

Other Application of

Ultrasound Elastography

### Section 3
