JBD · screening mammography, DCIS was a relatively uncommon presen-tation of breast cancer....

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JBDJournal of Breast Disease

Preoperative Breast Magnetic Resonance Imaging for the Assessment of the Size of Ductal Carcinoma In SituMusaed Rayzah, Jai Min Ryu, Jeong Eon Lee, Mansour Alramadhan, Bookyung Han1, Ha Woo Yi, Sungmin Park, Hyun-June Paik, Seok Jin NamDepartments of Surgery and 1Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea

Purpose: The purpose of this study was to determine whether magnetic resonance imaging (MRI) could assess the size of ductal carcinoma in situ (DCIS) more accurately compared to mammography and ultrasonography using the histopathological dimension of the surgical speci-men as the reference measurement. Methods: This was a retrospective review study using data from our institution database of breast can-cer. Preoperative contrast-enhanced MRI, mammography and ultrasonography were performed to detect and assess the size of DCIS in 131 patients. The greatest dimensions of DCIS determined by the imaging modalities were compared with the histopathological dimensions of the surgical specimens. Intraclass coefficients were calculated to examine the agreement among the MRI, mammography and ultrasonogra-phy measurements. The Wilcoxon signed-rank test was used to evaluate the statistical significance of the differences in size among MRI, mammography or ultrasonography and histopathology findings. Results: Of the 131 DCIS lesions, 126 (96.2%) were detected by MRI, 103 (78.6%) were detected by mammography, and 121 (92.4%) were detected by ultrasonography. The mean lesion size was 38.8 mm on histo-pathology, 36.0 mm on MRI, 28.8 mm on mammography, and 23.3 mm on ultrasonography, and there were no significant differences be-tween sizes determined by histopathology and MRI, while there were significant differences between histopathology and the other modali-ties. The correlation coefficient between histopathological measurement and MRI was 0.837, versus 0.461 between histopathology and mammography and 0.284 between histopathology and ultrasonography. The lesion size was correctly estimated (±5 mm), under-estimated (<5 mm), or over-estimated (>5 mm), respectively, by MRI in 52.7%, 30.5%, and 16.8% of cases; by mammography in 32.0%, 51.2%, and 16.8% of cases, respectively; and by ultrasonography in 24.4%, 62.6%, and 13.0% of cases, respectively. Conclusion: In our study, MRI was more accurate for detection and assessment the size of DCIS compared to mammography and ultrasonography.

Key Words: Breast neoplasms, Ductal carcinoma in situ, Magnetic resonance imaging

INTRODUCTION

Ductal carcinoma in situ (DCIS) is a noninvasive form of ductal car-

cinoma, limited to the confines of the basement membrane of the

duct. DCIS is a multiform disease with different growth patterns and a

heterogeneous set of clinical signs and symptoms [1]. Before the era of

screening mammography, DCIS was a relatively uncommon presen-

tation of breast cancer. However, since the introduction of mammog-

raphy screening programs for breast cancer, the incidence of DCIS has

risen consistently. DCIS currently accounts for 15% to 25% of all breast

cancers and 30% to 50% of all clinically occult cancers [2,3]. Approxi-

mately 40% of cases of DCIS evolve into invasive cancer [4].

Accurate information regarding the extent and distribution of

DCIS is important in determining the extent of surgery required.

Mammography is the primary tool of radiologists for the detection

and assessment of size of microcalcifications. However, mammogra-

phy is relatively limited in its ability to detect DCIS and assess tumor

size because it only detects the calcified portion of DCIS, and it can

underestimate or overestimate the histopathological tumor size. Con-

sequently, surgical resection is too often insufficient, resulting in a 30%

rate of re-excision because of persistent margin involvement [5], as well

as a higher risk of local recurrence [6,7].

Studies have shown that magnetic resonance imaging (MRI) is

more accurate than mammography for detecting and assessing tumor

size in patients with invasive cancer [8]. The sensitivity of MRI has

been reported to vary between 90% and 94% in larger studies and me-

ta-analyses [9,10]. However, few studies have investigated the value of

MRI for assessing the extent of DCIS; the initial results are encourag-

ORIGINAL ARTICLEJ Breast Dis 2016 December; 4(2): 77-84https://doi.org/10.14449/jbd.2016.4.2.77

Correspondence: Seok Jin NamDepartment of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul 06351, KoreaTel: +82-2-3410-3478, Fax: +82-2-3410-6982, E-mail: [email protected]: Mar 16, 2016 Revised: Apr 8, 2016 Accepted: Oct 24, 2016

http://www.jbd.or.kr https://doi.org/10.14449/jbd.2016.4.2.77

78 Musaed Rayzah, et al.

ing and demonstrate a fairly good correlation between size deter-

mined with MRI and histopathological size [11-13]. However, MRI of

the breast in patients with DCIS is not routinely performed and re-

mains experimental. Few studies have examined the effects of breast

MRI on surgical management specifically for DCIS [14-16].

The aim of this study was to evaluate the value of MRI for the stag-

ing of DCIS, and particularly for the accurate assessment of tumor

size in comparison with mammography and ultrasonography, using

the histopathological measurements as a reference.

METHODS

Patient selection

This was a single-center retrospective review from a Samsung

Medical Center database of breast cancer. All patients diagnosed with

pure DCIS, proven by core needle biopsy or vacuum-assisted biopsy,

between January 2013 and December 2014, were included. Patients

were excluded if they did not undergo MRI. Patients with multifocal

or multicentric lesions were also excluded because of the difficulty in

estimating the exact tumor size; thus, 131 patients were eligible for the

study. Data obtained for each patient included age; sex; and results of

the clinical breast examination, mammography, ultrasonography,

MRI, and histopathological examination of the biopsy and surgical

specimens. Clinical examination included the patient’s history, hor-

mone receptor status, and physical breast examination.

Imaging techniques

Mammography was performed using the Senographe 2000D sys-

tem (General Electric Medical Systems, Buc, France). Spot compres-

sion and magnification views were also obtained in patients with mi-

crocalcifications visible on mammography. Assessment of mammo-

grams considered breast density, and abnormalities were scored using

the Breast Imaging-Reporting and Data System (BI-RADS) mam-

mography classification [17].

Ultrasonography was performed systematically using the HDI

5000 (Advanced Technology Laboratories, Bothell, USA), iU22

(Philips Medical Systems, Bothell, USA) or LOGIQ700 (GE Medical

Systems, Milwaukee, USA), ultrasonography scanner, respectively

equipped with commercially available 12- to 7-MHz, and 10- to

7-MHz, linear-array transducers. The examinations were interpreted

using the BI-RADS ultrasonography classification system [18].

MRI was performed using a 1.5-T (Sigma; GE Healthcare, Milwau-

kee, USA) or 3.0-T (Philips Achieva; Philips Healthcare, Best, The

Netherlands) MRI system. Three-dimensional, fat-suppressed, gradi-

ent-echo, contrast material-enhanced, and dynamic images before

and seven times after a bolus injection of 0.1 mmol/kg of gadopen-

tetate dimeglumine (Magnevist; Berlex Laboratories, Wayne, USA)

were acquired in the sagittal or axial plane. The image acquisition

time per one dynamic scan was 60 to 90 seconds. Standard subtrac-

tion images were obtained by subtracting the precontrast images from

the early peak (or serial) postcontrast images on a pixel-by-pixel basis.

Reverse subtraction images were obtained by subtracting the last

postcontrast images from the early peak postcontrast images. Abnor-

malities were scored according to the BI-RADS MRI classification

system [19].

The findings obtained on all the imaging studies were analyzed,

and the size of the DCIS was measured as the single greatest measure-

ment by an experienced radiologist.

Biopsy, surgery, and histopathology

The diagnosis of DCIS was obtained via core needle biopsies or

vacuum-assisted biopsies, prior to the preoperative MRI and mam-

mography. All patients underwent surgery at our institution. Follow-

ing lumpectomy or mastectomy, gross specimens were reviewed by a

pathologist with expertise in breast pathology. The DCIS grade (high,

intermediate or low), presence or absence of microinvasive clusters or

an associated invasive tumor component, and nodal status were re-

corded. The histopathological size was recorded as the single greatest

measurement in one long axis dimension, regardless of the spatial

plane used.

Statistical analysis

Quantitative data are presented in a histogram, and as medians

with range and means and standard deviation (SD). The criterion

used for the accuracy of size assessment was a size within ± 5 mm

compared with the histological size. Two types of statistical analyses

were performed for correlations. Intraclass coefficients were calculat-

ed to examine the agreement between the MRI, mammography and

ultrasonography measurements and the histopathological size, with a

95% confidence interval. The Wilcoxon signed-rank test was used to

https://doi.org/10.14449/jbd.2016.4.2.77 http://www.jbd.or.kr

Preoperative Breast MRI for DCIS Assessment 79

evaluate the statistical significance of the differences in size between

MRI, mammography or ultrasonography and histopathology. A

p-value less than 0.05 was considered to indicate statistical signifi-

cance. All statistical analysis were performed using SAS version 9.4

(SAS Institute, Cary, USA). The requirement for informed consent

was waived because of the low risk posed by this investigation. This

study adhered to the ethical tenets of the Declaration of Helsinki and

was approved by the Institutional Review Board of Samsung Medical

Center in Seoul, Korea (IRB number: 2016-04-006).

RESULTS

The mean age ± SD was 48.6 ± 9.8 years overall (range, 35–78 years)

(Table 1); estrogen receptor expression was observed in 97 patients

(74.1%), while progesterone receptor expression was observed in 90

patients (68.7%). Of the 131 DCIS lesions, 126 (96.2%) were detected by

MRI, 103 (78.6%) were detected by mammography, and 121 (92.4%)

were detected by ultrasonography (Table 2).

The final histopathological study found 34 low-grade (26.0%), 59

intermediate-grade (45.0%), and 38 high-grade DCIS lesions (29.0%).

The mean histopathological size of the DCIS lesions was 38.8 mm (±

SD, 26.2 mm). The mean size of lesions determined by mammogra-

phy was 28.8 mm (± SD, 25.7 mm) (Table 1). The difference in the

mean size determined by mammography and histopathology was

-10.0 mm (± SD, 25.6 mm), a difference that was statistically signifi-

cant (p < 0.001) (Table 3). The graph showed wide variation between

sizes determined by mammography and histopathology (Figure 1).

The correlation coefficient between the histopathological size and

mammographic size was 0.461. Mammography correctly assessed the

lesion size (± 5 mm) in 33 cases (32.0%), underestimated the size in 53

cases (51.2%), and overestimated the size in 17 cases (16.8%) (Table 2).

Among our patient population, 25 patients (19.0%) had dense breasts

in which the lesions could not be visualized, while three patients

(2.3%) did not show lesions.

The mean ultrasonographic size of DCIS was 23.3 mm (± SD, 18.0

mm). The difference in mean size between ultrasonography and histo-

pathology was -15.6 mm (± SD, 23.9 mm), a difference that was statis-

tically significant (p < 0.001) (Table 3). The graph depicted a variation

between the ultrasonographic and histopathological sizes (Figure 1).

The correlation coefficient between the histopathological and ultraso-

nographic sizes was 0.284. Ultrasonography correctly assessed the le-

sion size (± 5 mm) in 29 cases (24.4%), underestimated the size in 76

cases (62.6%), and overestimated the size in 16 cases (13.0%) (Table 2).

The mean MRI size of the DCIS lesions was 36 mm (± SD, 24.3

mm). The difference in the mean size between MRI and histopathol-

ogy was -2.9 mm (± SD, 14.2 mm), a difference that was statistically

significant (p = 0.011) (Table 3). A close fit was graphically depicted

between the MRI and histopathological sizes (Figure 1). The size dis-

crepancy and span were smaller for the MRI measurements than for

the mammographic and ultrasonographic differences. The correla-

tion coefficient between the histopathological and MRI sizes was

Table 1. Mean age and mean size of DCIS as determined by ultrasonogra-phy, mammography, MRI, and histopathology

No. Mean SD

Age (yr) 131 48.6 9.8Pathology size (mm) 131 38.8 26.2Ultrasonography size (mm) 121 23.3 18.0Mammography size (mm) 103 28.8 25.7MRI size (mm) 126 36.0 24.3

DCIS = ductal carcinoma in situ; MRI = magnetic resonance imaging.

Table 2. Size assessment correlation coefficients between ultrasonographic, MRI imaging sizes and histological size

Ultrasonography Mammography MRI

No. of detection 121 103 126Sensitivity (%) 92.4 78.6 96.2Accurate estimation,

no. (%) 29 (24.4) 33 (32.0) 67 (52.7)

Under estimation ( < 5 mm), no. (%)

76 (62.6) 53 (51.2) 38 (30.5)

Over estimation ( > 5 mm), no. (%)

16 (13.0) 17 (16.8) 21 (16.8)

Correlation coefficient, all 0.284 0.461 0.837Nuclear grade Low 0.367 0.434 0.872 Intermediate 0.236 0.391 0.815 High 0.234 0.527 0.829

MRI = magnetic resonance imaging.

Table 3. Differences between ultrasonography, mammography or MRI as-sessments and histopathological assessment

Pathology difference No. Mean (mm) SD (mm) p-value

Ultrasonography 121 -15.6 23.9 < 0.001Mammography 103 -10.0 25.6 < 0.001MRI 126 -2.9 14.2 0.011

MRI = magnetic resonance imaging.



0.837. MRI correctly assessed the lesion size (± 5 mm) in 67 cases

(52.7%), underestimated the size in 38 cases (30.5%), and overestimat-

ed the size in 21 cases (16.8%) (Table 2). In patients with dense breast

tissue, MRI showed the lesion in 24 out of 25 patients.

According to histological grade, in low-grade DCIS, the mean size

determined by mammography was 21.4 mm (Table 4); the difference

between the mean mammographic size and the mean histopathologi-

cal size was -6.1 mm (± SD, 24.4 mm), which was not statistically sig-

nificant (p = 0. 067) (Table 5). On ultrasonography, the mean size was

19.5 mm; the difference between the mean ultrasonographic size and

the mean histopathological size was -8 mm (± SD, 18.1 mm), which

was not statistically significant (p = 0.067). On MRI, the mean size

was 27.3 mm; the difference in the mean MRI and histopathological

sizes was -0.2 mm (± SD, 10.3 mm), which was not statistically signifi-

cant (p = 0.758) (Table 5).

For intermediate grade DCIS, the mean size determined by mam-

mography was 28.1 mm (Table 4). The difference between the mean

mammographic size and the mean histopathological size was -13.5

12.5

10.0

7.5

5.0

2.5

0

12.5

10.0

7.5

5.0

2.5

0

12.5

10.0

7.5

5.0

2.5

0

12.5

10.0

7.5

5.0

2.5

0

0 2.5 5.0 7.5 10.0 12.5

0 2.5 5.0 7.5 10.0 12.5

0 2.5 5.0 7.5 10.0 12.5

0 2.5 5.0 7.5 10.0 12.5

Lesio

n siz

eLe

sion

size

Lesio

n siz

eLe

sion

size

Pathology tumor size

Ultra Mammogram MRI

Ultra

Mammogram

MRI




Figure 1. Correlation between the histopathological ductal carcinoma in situ (DCIS) size and corresponding DCIS size as measured by MRI, mammography and ultrasonography. Ultra=ultrasonography; MRI=magnetic resonance imaging.

Table 4. Mean size of DCIS by ultrasonography, mammography, and MRI and histopathological size according to histological grade

No.MRI size* (mm) Mammography size† (mm) Ultrasonography size‡ (mm) Pathology size (mm)

Mean SD Mean SD Mean SD Mean SD

Low 34 27.3 20.7 21.4 26.3 19.5 13.8 27.5 19.6Intermediate 59 36.4 25.0 28.1 25.3 20.9 17.8 41.6 28.5High 38 43.0 24.5 36.4 24.5 30.4 20.0 44.6 25.2

DCIS = ductal carcinoma in situ; MRI = magnetic resonance imaging.*5 Patients were excluded because they were not detected by MRI; †28 Patients were excluded because they were not detected by mammography; ‡10 Patients were excluded because they were not detected by ultrasonography.



mm (± SD, 27.7 mm), which was statistically significant (p < 0.001)

(Table 5). On ultrasonography, the mean size was 20.9 mm (Table 4).

The difference between the mean ultrasonographic and histopatho-

logical sizes was -20.8 mm (± SD, 24.5 mm), which was statistically

significant (p < 0.001) (Table 5). On MRI, the mean size was 36.4 mm

(Table 4). The difference between the mean MRI size and the mean

histopathological size was -5.24 mm (± SD, 15.6 mm), which was sta-

tistically significant (p = 0.007) (Table 5).

In high-grade DCIS, the mean size determined by mammography

was 36.4 mm (Table 4). The difference between the mean mam-

mographic and histopathological sizes was -8.2 (± SD, 23.3 mm),

which was statistically significant (p = 0.039) (Table 5). On ultrasonog-

Table 5. Differences between ultrasonography, mammography or MRI assessments and histopathological assessment according to histological grade

No.

MRI pathology difference* (mm)

Mammography pathology difference† (mm)

Ultrasonography pathology difference‡ (mm)

Mean SD p-value Mean SD p-value Mean SD p-value

Low 34 -0.2 10.3 0.758 -6.1 24.4 0.670 -8.0 18.1 0.067Intermediate 59 -5.2 15.6 0.007 -13.5 27.7 0.000 -20.8 24.5 0.000High 38 -1.6 14.6 0.392 -8.2 23.3 0.039 -14.3 26.0 0.001

MRI = magnetic resonance imaging.*5 Patients were excluded because they were not detected by MRI; †28 Patients were excluded because they were not detected by mammography; ‡10 Patients were excluded because they were not detected by ultrasonography.

Figure 2. A 48-year-old patient with an 18-mm ductal carcinoma in situ comedo type in her left breast that was more accurately assessed by magnetic reso-nance imaging (MRI). (A) Mediolateral mammography views showed a 13-mm calcification (arrow). (B) MRI showed a 19-mm nonmass enhancement (arrow). (C) Ultrasonography showed a 15-mm microcalcification.

B

CA



raphy, the mean size was 30.4 mm (Table 4). The difference between

the mean ultrasonographic and histopathological sizes was -14.3 mm

(± SD, 26.0 mm), which was statistically significant (p = 0.001) (Table

5). On MRI, the mean size was 43 mm (Table 4). The difference be-

tween MRI and histopathological sizes was -1.6 (± SD, 14.6 mm),

which was not statistically significant (p = 0.392). The correlation co-

efficient between the histopathological and MRI sizes was greater

than 0.8 for all grades, but this was not the case for the sizes deter-

mined by mammography or ultrasonography (Table 2).

DISCUSSION

The current study investigated the impact of MRI in preoperative

assessment of the size of DCIS compared with that of mammography

and ultrasonography. The findings showed that MRI assessed the ex-

tent of DCIS much more accurately than mammography and ultraso-

nography. Mammography is widely accepted as the most important

imaging method for the detection of DCIS, which is usually visualized

as clusters of microcalcifications [20]. However, its sensitivity was 78%

in the current study. In a prospective study of 167 cases of DCIS, Kuhl

et al. [21] reported a diagnostic sensitivity of only 56% with mammog-

raphy. In addition, the modality has some limitations in dense breasts,

which were found in 19% of participant in our study.

Ultrasonography is an adjunct modality used routinely in patients

diagnosed with DCIS. Previous studies [22,23] have reported the ul-

trasonographic features of DCIS as an architectural distortion, an in-

tracystic lesion or a bulky, hypoechoic vascular mass with ductal ex-

tension and prominent microlobules. In our study, DCIS was ob-

served as a nonmass abnormality, a round or oval-shaped, microlobu-

lated, mildly hypoechoic mass or a microcalcification (Figure 2), a re-

sult similar to those obtained in previous studies [22,23]. In addition,

microcalcification was also observed. The ability to visualize micro-

calcifications on ultrasonography has been described previously

[24,25]. In our study, ultrasonography detected DCIS lesions in 121

patients with a sensitivity of 92.4%. Lee et al. [25] reported the sensitiv-

ity of ultrasonography in DCIS as 86.5%.

MRI is not currently used as a systematic diagnostic modality in

DCIS, and controversy remains regarding its use for preoperative

planning. Previous studies have found that suspicious MRI findings

for DCIS include nonmass enhancement, especially in a ductal or seg-

mental/linear pattern, and variable perfusion patterns, including de-

layed washout, plateau, and persistent kinetics [26]. Although in our

study MRI showed enhancement in 126 patients, it showed nonmass

enhancement with an excellent sensitivity of 96% for DCIS detection.

Previous studies have reported sensitivities ranging from 60% to 100%

[12,13,27,28]. MRI is a useful adjunct modality for dense breast tissue;

in our study, it revealed the lesions in 96% of patients with dense

breasts and negative findings on mammography.

Regarding the preoperative size assessment of DCIS, mam-

mographic and ultrasonographic assessments of the lesion size were

mediocre in our study because the correlation coefficients between

these measurements and the size determined by histology were only

0.461 and 0.284, respectively. In our study, mammography tended to

underestimate the size of DCIS. This finding did not differ signifi-

cantly from those reported in the literature [29]. Furthermore, in our

study, ultrasonography tended to underestimate the size of lesions by

10% compared to mammography.

Can MRI palliate the limitations of mammography and ultraso-

nography to serve as an effective tool for the staging of DCIS? The

correlation coefficient between size determined by MRI and size de-

termined by histology in our study was very satisfactory (0.837), with

excellent reliability. MRI accurately estimated the DCIS size in 52.7%

of cases. Other studies [11-13,30], which included 30, 22, 72, and 33

patients, respectively, all reported accurate MRI estimation of size in

57% to 72% of cases. Only a few studies [11,30] considered an accurate

size assessment as one that was within ± 5 mm. In the study of

Schouten van der Velden et al. [30], size assessment with MRI was ac-

curate in 38% of cases versus 27% with mammography, with no statis-

tical significance; however, in the study of Marcotte-Bloch et al. [11],

size assessment had an accurate rate of 60% with MRI versus 38% with

mammography (this difference was statistically significant).

The results obtained in our study showed statistical significance in

favor of better size assessment for all histological grades of DCIS by

MRI compared with size determinations by mammography and ul-

trasonography. However, our study had limitations. First, it employed

a retrospective design, with data from a single institution. Second,

multicentric or multifocal cancer was excluded, possibly limiting the

reliability of the results. Third, breast images were performed after

core needle or vacuum-assisted biopsies, generating a bias in imaging

and pathological measurements. Fourth, all lesions analyzed were



pure DCIS in the final histopathology; lesions with associated micro-

invasive or invasive clusters were also included. Despite these limita-

tions, our findings are significant and warrant further investigations.

In conclusion, our study confirmed that preoperative MRI staging

of DCIS assessed the extent of these tumors much more accurately

than mammography and ultrasonography. Precise preoperative as-

sessment of tumor size should improve surgical planning and reduce

the risk of secondary recurrence.

CONFLICT OF INTEREST

The authors declare that they have no competing interests.

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