**1. Introduction**

22 Imaging of the Breast – Technical Aspects and Clinical Implication

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#### **1.1 Increase incidence of breast cancer in Taiwan and Asia**

Although the incidence of breast cancer is lower in Asian countries, the cause-specific mortality in most Asian countries is much higher as compared to western countries (Agarwal et al., 2007; Shibuya et al., 2002). Although the overall picture of breast cancer is variable among different Asian countries and in different ethnic groups within individual countries, breast cancer has emerged as the largest cancer problem in Asian women. Breast cancer is also the largest cause of cancer-related deaths. It remains the second commonest malignancy in women in the rural areas of developing Asian countries (Agarwal et al., 2007). Breast cancer is gradually become one of the major public health problem and the most important issue to concern in order to decrease cancer mortality.

Base on the data from the Bureau of Health Promotion, Department of Health, Executive Yuan, Taiwan, indicate that the incidence of breast cancer in Taiwan increased from 27.9 to 49.2 per 100,000 women in the decade from 1995 to 2005, which is an annual increase of approximately 7%. As the decrease incidence of cervical cancer in the meanwhile, breast cancer is already the highest new number of malignancy diagnosis in Taiwan. Moreover, according to the data released from the World Health Organization, an incidence of Taiwanese breast cancer is reported as 52.8 per 100,000 women in 2008, which is the second place in Asia, only slightly lower than that seen in Singapore.

#### **2. Characteristics and difficulty of early detection of breast tumor in Asian women**

There are higher proportions of breast cancer patients in developing Asian countries are younger than patients in developed Asian and western countries (Agarwal et al., 2007; Amr et al., 1995). Given the huge population in the developing Asian nations, and the fact that up to 25% of all breast cancer patients in Asian countries are young, and also, young age by itself is a known indicator of poor prognosis in breast cancer patients (Agarwal et al., 2007; Amr et al., 1995). The first nation-wide mammographic screening program in Asia was started in Singapore during 2002 (Chuwa et al., 2009). By 2009, there is still no significant survival benefit could be demonstrated in the country, in the meanwhile, rapid increase of breast cancer incidence was reported. Singapore government choose for longer period of

The Application of Breast MRI on Asian Women (Dense Breast Pattern) 25

and investigated whether the women with DBPP should receive more frequent screening or screening with alternative techniques that increase the length of the preclinical detectable

Data collected in Japan showed the successful result of a mass screening program using mammography on asymptomatic women over 50 years of age. The program had a 0.84 % cancer detection rate. The breast cancer cases screened from the program had not been detected by physical examination (Morimoto et al., 1994). The detection rates were higher in

In a study of Japanese women, mammography missed 16 % of breast cancer occurrences (Uchida et al., 2008). Breast density was also confirmed as a significant determinant of breast cancer risk. They quantitatively measured the mammographic density, and found that a higher risk was associated with a larger breast size and with a higher proportion of glandular density, especially for extreme densities (Nagata et al., 2005). A study in Singapore showed an increased risk of breast cancer associated with a higher-density pattern with extensive nodular characteristics, and linear densities with a nodular size larger

Although breast cancer is the most common female cancer in South Korea, its early detection rate is low compared to developed Western countries (Ryu et al., 2008). The clinical characteristics of Korean breast cancer patients showed a pattern of a younger age (< 50 years old) and increasing early stage and asymptomatic cases. This finding reflects the need for more effective breast screening programs for young Korean women (Son et al.,

Increased breast parenchyma density correlates with breast cancer risk and obscures the detection with the mammography of early stage, small-sized breast tumors. Asian women have smaller breasts and are affected by breast cancer at a younger age; both factors that are

**3. Limitation of conventional mammography in detecting early tumors in** 

In Western countries, mammography has been proven to detect breast cancer at an early stage and, when followed up with appropriate diagnosis and treatment, to reduce the

Asian women have higher breast densities than Caucasian women, in addition, mammography is not a perfect screening tool for Asian women with DBPP. Mammography has lower sensitivity for invasive ductal carcinoma of breasts in patients with DBPP (Kolb et

The percentage of dense tissue to breast volume of both Chinese and Japanese women appeared to be higher than that in Caucasian women (Maskarineca et al., 2001). Despite the considerably smaller proportion of non-dense areas, the overall proportion of dense breast tissue in the breasts of Chinese and Japanese women is 20 % higher than in Caucasian women in the same age group (Huang et al., 2001; Maskarineca et al., 2001). Irrespective of

race, women with lower mammographic densities have a lower risk of breast cancer.

**young Asian women with dense breast parenchyma pattern** 

mortality rate caused by breast cancer (Saslow et al., 2007).

phase to reduce breast cancer mortality (Van Gils et al., 1999).

the sixth and seventh decades of life.

than normal lobules (Jakes et al., 2000).

associated with DBPP (Leung et al., 2010b).

2006).

al., 2002).

follow-up, expect for the benefit of mortality reduction in the population resulted from their mass mammography screening program (Chuwa et al., 2009). As we know, many therapeutic options for early detected breast cancer with small tumor size, the success rate of therapy for early stage cancer is higher than advanced stage disease.

In Taiwan, a national project of 2-year interval screening mammograms for 45- to 70-yearold women has detected significantly more early breast cancers (Chen et al., 2008). However, the major source of breast cancer detection is not arise from this screening program. The overall average detection size of breast cancer tumors in Taiwan is over 2 cm, which is larger than that detectable with the diagnostic capabilities in Europe and North America (Ng et al., 1998; Shen et al., 2005). The median age at diagnosis of breast cancer is 45–49 years in Taiwan, and this age group is more likely to present with a dense breast parenchyma pattern (DBPP). This median age is significantly lower than that of Caucasian women in Western countries, where breast cancer peaks between the ages of 70 and 74 years, and this older age group is more likely to present with a non-dense parenchyma pattern (NDBPP) (Huang et al., 2001; Shen et al., 2005). Breast cancer in this age group is reportedly more aggressive (Kwong et al., 2008). This pathological pattern is also commonly seen in our clinical practice in Taiwan (Leung et al., 2010b). Previous study have demonstrated that the prevalence of NDBPP (ACR types 1 and 2; ACR: American College of Radiology classification of breast parenchymal density in digital mammography) could be as high as 78%, compared with 22% for DBPP (ACR types 3 and 4), which is representative of most Western countries (Table 1) (Van Gils et al., 1999). The ratio of NDBPP to DBPP is reversed compared with their previous results. Although the case number is small, we believe that the results are representative of developed Asian countries such as Taiwan, Hong Kong, South Korea, Singapore, and Japan.


Table 1. Analysis of the prevalence of breast pattern in Taiwan and Western countries (Leung et al., 2010b; Van Gils et al., 1999).

Breast density is a major factor influencing the incidence of breast malignancy, and has been discussed extensively in the past two decades. In a normal woman, mammographic densities correspond to different amounts of fat and connective and epithelial tissue. Fat appears radiographically dark on film-screen mammograms, and radiographically opaque areas represent epithelial and connective tissues (Gram et al., 1997). Most cases of high mammographic density are not abnormalities, but varied distributions in healthy breast tissue. It was also found that high mammographic density may be related to a fourfold increased risk of developing breast cancer. It was found that the diagnostic sensitivity of mammography in women with a fatty breast pattern is 98% (Boyd et al., 1998; Kolb et al., 2002). Women with high mammographic breast densities are at higher risk of breast cancer; the incidence of breast cancer in NDBPP was 26.4% versus 73.4% in DBPP. It was discussed

follow-up, expect for the benefit of mortality reduction in the population resulted from their mass mammography screening program (Chuwa et al., 2009). As we know, many therapeutic options for early detected breast cancer with small tumor size, the success rate of

In Taiwan, a national project of 2-year interval screening mammograms for 45- to 70-yearold women has detected significantly more early breast cancers (Chen et al., 2008). However, the major source of breast cancer detection is not arise from this screening program. The overall average detection size of breast cancer tumors in Taiwan is over 2 cm, which is larger than that detectable with the diagnostic capabilities in Europe and North America (Ng et al., 1998; Shen et al., 2005). The median age at diagnosis of breast cancer is 45–49 years in Taiwan, and this age group is more likely to present with a dense breast parenchyma pattern (DBPP). This median age is significantly lower than that of Caucasian women in Western countries, where breast cancer peaks between the ages of 70 and 74 years, and this older age group is more likely to present with a non-dense parenchyma pattern (NDBPP) (Huang et al., 2001; Shen et al., 2005). Breast cancer in this age group is reportedly more aggressive (Kwong et al., 2008). This pathological pattern is also commonly seen in our clinical practice in Taiwan (Leung et al., 2010b). Previous study have demonstrated that the prevalence of NDBPP (ACR types 1 and 2; ACR: American College of Radiology classification of breast parenchymal density in digital mammography) could be as high as 78%, compared with 22% for DBPP (ACR types 3 and 4), which is representative of most Western countries (Table 1) (Van Gils et al., 1999). The ratio of NDBPP to DBPP is reversed compared with their previous results. Although the case number is small, we believe that the results are representative of developed Asian countries such as Taiwan,

NDBPP DBPP

20.8 79.2

78 22

Table 1. Analysis of the prevalence of breast pattern in Taiwan and Western countries

Breast density is a major factor influencing the incidence of breast malignancy, and has been discussed extensively in the past two decades. In a normal woman, mammographic densities correspond to different amounts of fat and connective and epithelial tissue. Fat appears radiographically dark on film-screen mammograms, and radiographically opaque areas represent epithelial and connective tissues (Gram et al., 1997). Most cases of high mammographic density are not abnormalities, but varied distributions in healthy breast tissue. It was also found that high mammographic density may be related to a fourfold increased risk of developing breast cancer. It was found that the diagnostic sensitivity of mammography in women with a fatty breast pattern is 98% (Boyd et al., 1998; Kolb et al., 2002). Women with high mammographic breast densities are at higher risk of breast cancer; the incidence of breast cancer in NDBPP was 26.4% versus 73.4% in DBPP. It was discussed

therapy for early stage cancer is higher than advanced stage disease.

Hong Kong, South Korea, Singapore, and Japan.

(Leung et al., 2010b; Van Gils et al., 1999).

Breast pattern according to

Prevalence (%) in Taiwan (Leung et al in Taipei Medical

university Hospital)

Prevalence (%) in Western countries

mammography

and investigated whether the women with DBPP should receive more frequent screening or screening with alternative techniques that increase the length of the preclinical detectable phase to reduce breast cancer mortality (Van Gils et al., 1999).

Data collected in Japan showed the successful result of a mass screening program using mammography on asymptomatic women over 50 years of age. The program had a 0.84 % cancer detection rate. The breast cancer cases screened from the program had not been detected by physical examination (Morimoto et al., 1994). The detection rates were higher in the sixth and seventh decades of life.

In a study of Japanese women, mammography missed 16 % of breast cancer occurrences (Uchida et al., 2008). Breast density was also confirmed as a significant determinant of breast cancer risk. They quantitatively measured the mammographic density, and found that a higher risk was associated with a larger breast size and with a higher proportion of glandular density, especially for extreme densities (Nagata et al., 2005). A study in Singapore showed an increased risk of breast cancer associated with a higher-density pattern with extensive nodular characteristics, and linear densities with a nodular size larger than normal lobules (Jakes et al., 2000).

Although breast cancer is the most common female cancer in South Korea, its early detection rate is low compared to developed Western countries (Ryu et al., 2008). The clinical characteristics of Korean breast cancer patients showed a pattern of a younger age (< 50 years old) and increasing early stage and asymptomatic cases. This finding reflects the need for more effective breast screening programs for young Korean women (Son et al., 2006).

Increased breast parenchyma density correlates with breast cancer risk and obscures the detection with the mammography of early stage, small-sized breast tumors. Asian women have smaller breasts and are affected by breast cancer at a younger age; both factors that are associated with DBPP (Leung et al., 2010b).

#### **3. Limitation of conventional mammography in detecting early tumors in young Asian women with dense breast parenchyma pattern**

In Western countries, mammography has been proven to detect breast cancer at an early stage and, when followed up with appropriate diagnosis and treatment, to reduce the mortality rate caused by breast cancer (Saslow et al., 2007).

Asian women have higher breast densities than Caucasian women, in addition, mammography is not a perfect screening tool for Asian women with DBPP. Mammography has lower sensitivity for invasive ductal carcinoma of breasts in patients with DBPP (Kolb et al., 2002).

The percentage of dense tissue to breast volume of both Chinese and Japanese women appeared to be higher than that in Caucasian women (Maskarineca et al., 2001). Despite the considerably smaller proportion of non-dense areas, the overall proportion of dense breast tissue in the breasts of Chinese and Japanese women is 20 % higher than in Caucasian women in the same age group (Huang et al., 2001; Maskarineca et al., 2001). Irrespective of race, women with lower mammographic densities have a lower risk of breast cancer.

The Application of Breast MRI on Asian Women (Dense Breast Pattern) 27

malignancy could not be concluded due to a dense breast parenchyma background. However, breast MRI with a subtraction image demonstrated an enhanced tumor mass.

(a) (b)

(c) Fig. 1. (a) Mammogram of the non-dense parenchyma pattern group shows a large tumor and cluster of microcalcifications (thin white arrow) at the superior left breast with enlarged lymph nodes (thick white arrow), which was diagnosed as advanced infiltrative ductal carcinoma and lymph node metastasis. (b) The corresponding breast magnetic resonance imaging subtracted image of ESP (white arrow) matched the mammographic interpretation. (c) It shows a characteristic "wash-out" enhancing curve pattern, which is more likely to

appear in malignancy.

Whether the presence of many dense areas in the breasts corresponds to a higher cancer risk is unclear (Boyd et al., 2005; Kolb et al., 2002; Maskarineca et al., 2001; Tseng et al., 2006). In fact, mammographic density usually reflects the opacity of epithelial and stromal tissue in the breast within the lucent background of non-dense fatty tissue. Ductal carcinoma *in situ* and infiltrative ductal carcinomas originate in epithelial cells, and therefore, areas of fibroglandular tissue with a greater number of cells are at a higher risk during increased epithelial proliferation (McCormack & Santos et al., 2006). The masking hypothesis proposed by Egan and Mosteller (1977) may also explain why radiographically dense patterns are associated with an increased risk of breast cancer. They found that breast cancer was easy to detect using mammography in breasts with non-dense glandular parenchyma, though it was unreliable for detecting cancer in dense glandular parenchyma. Cases of missed cancer detection during a first mammographic examination due to the masking effect of dense glandular tissue of the breast may be detected in subsequent mammographic examinations. The apparent excess of cancers detected in this specific group, with initial masking of the tumor in dense breasts, can cause the group to appear to be at a higher risk than those with non-dense breast tissue (Leung et al., 2010). Conventional mammography is also lower sensitivity to detect enlarged axillary and have no information on internal mammary chain. Probably due to some additional reasons, such as the screening program may cause call-back anxiety, psychological trauma by false positive results and radiation exposure (Leung et al., 2002), Hong Kong and most regions of mainland China currently have no mass screening programs for any age group.

Although some limitations of mammographic screening on DBPP women in Asia, we need give applause to health policy planners in the majority of developed Asian countries, such as Japan, Singapore, Taiwan, and South Korea, are believed helping us to bring early breast cancer awareness and provide cost-effective screening to prevent delay diagnosis of Asian breast cancer.

#### **4. Application of breast MRI on Asian women and the dense breast parenchyma pattern**

Digital mammography is reliable as a screening or diagnostic tool for Asian women with NDBPP. Mammography can reliably image microcalcifications and solid tumors with good contrast from the fatty background tissue of the breast. The aim of image production during mammography is to separate fatty tissue from glandular breast tissue of low contrast density based on different X-ray absorption characteristics. Mammographic density estimation is based on a single two-dimensional projection of the breast. In contrast, breast MRI distinguishes different tissue types based on their signal production after radiofrequency stimulation within a strong magnetic field. MRI evaluation of the breast is three-dimensional, and the image analysis is assisted by a post-enhanced kinetic curve, and subtraction techniques only allow contrast-enhanced lesions to be depicted (Figures 1&2).

Figure 1 presents a representative case in the NDBPP group showing that a large tumor and cluster of microcalcifications could be easily detected with both mammography and breast MRI. Figure 2, in contrast, shows a representative case from the DBPP group. The mammograms of the left breast under cranial-caudal and medial-oblique views show diffuse faint nodular shadows without major architectural distortion. The finding of

Whether the presence of many dense areas in the breasts corresponds to a higher cancer risk is unclear (Boyd et al., 2005; Kolb et al., 2002; Maskarineca et al., 2001; Tseng et al., 2006). In fact, mammographic density usually reflects the opacity of epithelial and stromal tissue in the breast within the lucent background of non-dense fatty tissue. Ductal carcinoma *in situ* and infiltrative ductal carcinomas originate in epithelial cells, and therefore, areas of fibroglandular tissue with a greater number of cells are at a higher risk during increased epithelial proliferation (McCormack & Santos et al., 2006). The masking hypothesis proposed by Egan and Mosteller (1977) may also explain why radiographically dense patterns are associated with an increased risk of breast cancer. They found that breast cancer was easy to detect using mammography in breasts with non-dense glandular parenchyma, though it was unreliable for detecting cancer in dense glandular parenchyma. Cases of missed cancer detection during a first mammographic examination due to the masking effect of dense glandular tissue of the breast may be detected in subsequent mammographic examinations. The apparent excess of cancers detected in this specific group, with initial masking of the tumor in dense breasts, can cause the group to appear to be at a higher risk than those with non-dense breast tissue (Leung et al., 2010). Conventional mammography is also lower sensitivity to detect enlarged axillary and have no information on internal mammary chain. Probably due to some additional reasons, such as the screening program may cause call-back anxiety, psychological trauma by false positive results and radiation exposure (Leung et al., 2002), Hong Kong and most regions of mainland China currently

Although some limitations of mammographic screening on DBPP women in Asia, we need give applause to health policy planners in the majority of developed Asian countries, such as Japan, Singapore, Taiwan, and South Korea, are believed helping us to bring early breast cancer awareness and provide cost-effective screening to prevent delay diagnosis of Asian

Digital mammography is reliable as a screening or diagnostic tool for Asian women with NDBPP. Mammography can reliably image microcalcifications and solid tumors with good contrast from the fatty background tissue of the breast. The aim of image production during mammography is to separate fatty tissue from glandular breast tissue of low contrast density based on different X-ray absorption characteristics. Mammographic density estimation is based on a single two-dimensional projection of the breast. In contrast, breast MRI distinguishes different tissue types based on their signal production after radiofrequency stimulation within a strong magnetic field. MRI evaluation of the breast is three-dimensional, and the image analysis is assisted by a post-enhanced kinetic curve, and subtraction techniques only allow contrast-enhanced lesions to be depicted

Figure 1 presents a representative case in the NDBPP group showing that a large tumor and cluster of microcalcifications could be easily detected with both mammography and breast MRI. Figure 2, in contrast, shows a representative case from the DBPP group. The mammograms of the left breast under cranial-caudal and medial-oblique views show diffuse faint nodular shadows without major architectural distortion. The finding of

**4. Application of breast MRI on Asian women and the dense breast** 

have no mass screening programs for any age group.

breast cancer.

(Figures 1&2).

**parenchyma pattern** 

malignancy could not be concluded due to a dense breast parenchyma background. However, breast MRI with a subtraction image demonstrated an enhanced tumor mass.

Fig. 1. (a) Mammogram of the non-dense parenchyma pattern group shows a large tumor and cluster of microcalcifications (thin white arrow) at the superior left breast with enlarged lymph nodes (thick white arrow), which was diagnosed as advanced infiltrative ductal carcinoma and lymph node metastasis. (b) The corresponding breast magnetic resonance imaging subtracted image of ESP (white arrow) matched the mammographic interpretation. (c) It shows a characteristic "wash-out" enhancing curve pattern, which is more likely to appear in malignancy.

The Application of Breast MRI on Asian Women (Dense Breast Pattern) 29

Mammography has well-recognized limitations for early breast cancer detection, especially for Asian women with DBPP. In the United States, MRI is provided as an adjunctive screening tool, mainly for women who may be at increased risk for the development of breast cancer. The Society of Breast Imaging and the Breast Imaging Commission of the ACR issue these recommendations to provide guidance to patients and clinicians on the use of imaging to screen for breast cancer. The recommendations are based on available evidence, or based on consensus opinions of professionals and experts from the executive committee of the Society of Breast Imaging and the members of the Breast Imaging Commission of the ACR. These recommendations are intended to suggest appropriate utilization of breast MRI for screening high-risk groups. They are not intended to replace sound clinical judgment and are not to be construed as representing the standard of care. Mammography should be remembered to be the only imaging modality that has been proven to decrease mortality from breast cancer. Before using breast MRI, the potential benefits, limitations, and harm from this additional screening modality should be reviewed (Lee et al., 2010; Saslow et al.,

Similar to Western countries, a higher proportion of Asian women with breast cancer have at least one relative with breast cancer. This risk can be almost double that of the general population. However, the gene correlated with this is different from that found in Western countries. In addition, gene screening programs and services are poorly developed, even in the wealthiest Asian countries. To define the high-risk group in the population, the national screening mammography program in Taiwan provides services for women aged between 40-45 years with a family history of breast cancer. Considering the low sensitivity of mammography in young women, a more aggressive breast MRI screening at this age or lower is recommended. Adjuvant breast MRI screening should also be considered for women with lymphoma (Hodgkin's disease), women who received radiation treatment between the ages of 10 to 30 years, women with lobular carcinoma *in situ* (LCIS), atypical lobular hyperplasia (ALH), and atypical ductal hyperplasia (ADH), which may range from normal ductal hyperplasia to ductal carcinoma *in situ* (DCIS). Specifically, women with a personal history of breast cancer, including DCIS, should be included. As previously mentioned, DBPP has been shown to be an independent risk factor for breast cancer. Women with the highest breast density were found to have a 4- to 6-fold increased risk compared with women with the least dense breasts. In addition, malignant tumors of the breast are more likely to arise in the areas of greatest mammographic density than in fattier areas of the breast. Although the ACS recommendations for Breast MRI Screening as an adjunct to mammography are more detailed, the most suitable indications for Asian women

are provided in the following table (**Table 2**; Lee et al., 2010; Saslow et al., 2007)

malignancy (Dorrius et al., 2009; Dorrius et al., 2010).

**6. The value of breast MRI as an adjunct in the diagnosis of breast diseases**  Breast MRI can be used as an adjunct in the diagnosis of breast diseases when inconclusive findings in conventional imaging exist, such as with mammography and sonography (BI-RADS 0). Therefore, MRI can be used as a problem-solving modality (Mann et al., 2008). Generally, breast MRI provides a relatively higher negative predictive value for excluding

**5. MRI acts as a screening tool in a population of asymptomatic women** 

2007).

Fig. 2. Mammograms of the left breast under (a) cranial-caudal and (b) medial-oblique views of the dense parenchyma pattern group show diffuse faint nodular shadows without major architectural distortion. The finding of malignancy could not be concluded due to a dense breast parenchyma background. (c) However, follow-up breast magnetic resonance imaging with a subtraction image of ESP demonstrated an enhanced tumor mass (white arrow) at the medial aspect. (d) The corresponding enhanced curve analysis revealed a characteristic "wash-out" pattern.

(d)

Because the image is processed by subtraction of all the background tissue, a possible lesion can only be identified in the presence of extremely dense glandular tissue, different types of implantation, or fibrotic changes after chemotherapy with BRMRI (Thompson et al., 2009).

Previous study conducted by Kuhl et al (2010), have indicated that breast MRI is significantly more sensitive than mammography, sonography, and a combination of both. Breast MRI and mammography are more specific than sonography alone or in combination. In addition, the positive predictive value of breast MRI was 48%, higher than 39% of mammography and 36% of ultrasound.

(a) (b) (c)

"wash-out" pattern.

mammography and 36% of ultrasound.

(d) Fig. 2. Mammograms of the left breast under (a) cranial-caudal and (b) medial-oblique views of the dense parenchyma pattern group show diffuse faint nodular shadows without major architectural distortion. The finding of malignancy could not be concluded due to a dense breast parenchyma background. (c) However, follow-up breast magnetic resonance imaging with a subtraction image of ESP demonstrated an enhanced tumor mass (white arrow) at the medial aspect. (d) The corresponding enhanced curve analysis revealed a characteristic

Because the image is processed by subtraction of all the background tissue, a possible lesion can only be identified in the presence of extremely dense glandular tissue, different types of implantation, or fibrotic changes after chemotherapy with BRMRI (Thompson et al., 2009). Previous study conducted by Kuhl et al (2010), have indicated that breast MRI is significantly more sensitive than mammography, sonography, and a combination of both. Breast MRI and mammography are more specific than sonography alone or in combination. In addition, the positive predictive value of breast MRI was 48%, higher than 39% of
