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European Journal of Radiology 167 (2023) 111053
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European Journal of Radiology

journal homepage: www.elsevier.com/locate/ejrad
Breast MRI – The champion in the millimeter league

MIO breast MRI – The method of choice in women with dense breasts
Uwe Fischer
Diagnostic Breast Care Center, Bahnhofsallee 1d, 37081 Goettingen, Germany
A R T I C L E I N F O A B S T R A C T
Keywords: We perform MRI of the breast as a first pass technique. We successfully established 10-minute-protocols
Breast Carcinoma (including T2 images) with a fixed dosage of 5 ml 1 M CM. A high spatial resolution of 526 × 526, better
MRI 672 × 672 or maximum (1.024 × 1.024, MIO MRI) is vital to achieve best results. We use fixation tools to avoid
Breast MRI
motion artifacts. Motion correction algorithms can, however, often eliminate such artifacts when they are pre
MR-guided intervention
sent. In initial breast MRI exams, morphologic features are the most important criteria for lesion evaluation. If
previous exams are available for comparison, the main criteria indicating a suspicious lesion are an increase in
lesion size or the depiction of new lesions.
High quality HR MRI of the breast is the method of choice in women with dense or extremely dense breasts in
all cases (screening, assessment, follow up). In density type A or B, MRI can be helpful in defined constellations,
e.g. when MX and US are limited or contraindicated.
According to our experience, 95% or more of all carcinomas of the breast are detectable on MRI. The
remaining 5% of MRI-occult lesions are intraductal tumors or very small invasive carcinomas depicted with
mammography due to associated microcalcifications. MRI is, however, superior to all other imaging modalities in
the detection of the clinically relevant DCIS (high risk DCIS, intermediate type).
Consecutive MRI examinations in intervals of 12 to 24 months allow a reliable detection of invasive breast
cancer with an average size of 7–8 mm. This corresponds to a rate of metastasis-free locoregional lymph nodes in
>95% of cases. The rate of interval cancers is <2%. In conclusion, this strategy may increase the overall-lifetime
survival of breast cancer patients to more than 95%. Inversely, mortality may be reduced to <5%.
Taking these improvements in early breast cancer detection and survival that can be achieved through the
implementation of QA HR MRI of the breast into account, it should be discussed to modify oncologic guidelines
for the treatment of breast cancer.
MRI is the best diagnostic tool we have and according to our experience, a first pass, quality-assured high-
resolution breast MRI protocol provides best diagnostic results at minimal procedural effort.
1. Introduction nodes (<5%), thus staged as pN0.

While undetected invasive breast cancer usually leads to death, DCIS
The purpose of diagnostic imaging of the breast is the detection of must be discussed in more detail because DCIS of different histologic
breast cancer at an early stage. This means detecting an invasive grades are associated with different prognoses. In contrast to low-grade
carcinoma that is <10 mm in diameter or detecting a non-invasive, DCIS, tumor cells of intermediate type and especially high-grade DCIS
intraductal breast tumor (DCIS). Breast cancers diagnosed at a pT1a, will leave the duct and progress to an invasive carcinoma. Low-grade, in
pT1b, or pTis histologic stage have an excellent lifetime survival contrast, usually remains intraductal for many decades, and most of the
prognosis and are very rarely associated with metastases to the lymph women do not fall ill from this tumor entity. Thus, it is actually
Abbreviations: ACR, American College of Radiology; ADC, Apparent diffusion coefficient; AI, Artificial intelligence; ABB-MRI, Abbreviated MRI; BCT, Breast
conserving therapy; BPE, Background parenchymal enhancement (in MRI); BW, Body weight; CEBCT, Contrast-enhanced breast computer tomography; CEM,
Contrast-enhanced mammography; CEMRI, Contrast-enhanced magnetic resonance imaging; CM, Contrast material; CUP, Carcinoma of unknown primary; DTS,
Digital tomosynthesis; EIC, Extensive intraductal component; EPI, Echo planar imaging; FS, Fat saturated; FGT, Fibroglandular tissue (in MRI); G, Gauge; Gd,
Gadolinium; HR, High resolution; IR, Inversion recovery; MIP, Maximum intensity projection; MX, Mammography; QA, Quality assured; US, Ultrasound; y, Years.
E-mail address: [email protected].
https://doi.org/10.1016/j.ejrad.2023.111053
Received 8 August 2023; Accepted 16 August 2023
Available online 24 August 2023
0720-048X/© 2023 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
U. Fischer European Journal of Radiology 167 (2023) 111053
Fig. 1. Distribution of breast density types 1–4 in women aged 50y to 70y. Women of screening-relevant age show dense (Stufe 3, ACR C) or extremely dense
(Stufe 4, ACR D) breast tissue (from [8] in 50% of cases).
Fig. 2. MRI open breast coil. Dedicated bilateral open breast surface coil with integrated fixation unit (Noras company, Höchberg, Germany).
Fig. 3. Compression device. Integrated fixation tool with two non-curved compression paddles, non-compressed status (Noras company, Höchberg, Germany).
questionable as to whether or not the detection of low-grade DCIS is and D), however, the sensitivity of mammography for the detection of
important, or whether its’ detection constitutes an over-diagnosis with breast cancer decreases to 32–45% [1–2]. The additional performance of
consecutive over-treatment. breast ultrasonography in such cases can increase the sensitivity up to
Currently, three imaging modalities are being used for the early 65% [3–4]. Breast ultrasound as a stand-alone-technique is not adequate
detection of breast cancer. These are mammography (including tomo for the reliable detection of breast cancer at an early stage [5]. Even
synthesis, DTS and CE mammography, CEM), ultrasonography, and CE tomosynthesis is not able to increase the sensitivity of mammography
breast MRI. Mammography is efficient in the depiction of solid lesions significantly [6–7]. The low sensitivity of mammography and tomo
within breasts with low parenchymal density and in the detection of synthesis, with or without ultrasound for women with dense and
cancers associated with microcalcifications in all density types. In extremely dense breast tissue is a problem for about 50% of women in a
breasts with high or extremely high parenchymal density (type ACR C breast-cancer relevant age group (Fig. 1) [8].
2
Fig. 4. Positioning for Breast MRI. Prone position of the patient with both breasts hanging in the open breast coil. Arms lay along the body with fixation in the
dressing gown’s belt loop to promote relaxation of the pectoral muscles. Antegrade positioning of the head holder with integrated mirror to look out. Headset
with music.
Fig. 5. a,b: Intraindividual comparison of different CM dosages. 68-year-old woman with an oval, well-defined mass with endotumoral dark septations in the
retromamillary region. Equivalent presentation of the mass in subtraction image of MRI with 5 ml CM (initial signal increase: 66%)(a), and a few days later with
body-weighted dosage (9 ml; 90 kg BW) (initial signal increase: 37%)(b). Histology: Fibroadenoma.
The only way to solve this problem is the use of contrast-enhanced amount of parenchymal tissue does not correlate with the perfusion in
methods. CE imaging is based on the visualization of tumorangio the breast. Aspects that do have influence on the intensity of paren
genesis. Folkman et al. have shown that all invasive breast cancers > chymal perfusion i.e. enhancement are the cardial output and the level
2–3 mm initiate pathologic angiogenesis [9–10]. For DCIS it could be of hormonal influence. Increased hormonal parenchymal enhancement
demonstrated that there is an increased uptake of contrast material, can be seen in certain phases of the menstrual cycle of premenopausal
especially for high-grade DCIS. The clinically less relevant low-grade women, and in women receiving hormone replacement therapy
DCIS, on the other hand, can be missed with CE imaging methods [12–15].
[11]. Thus CE imaging methods allow the reliable depiction of breast Compared to CEM and CE breast CT (CEBCT), CE MRI is the most
cancer in all breast density types (including dense breasts) because the established method and has been used since nearly 50 years. CEM has
3
Fig. 6. a,b: Intraindividual comparison of different CM dosages. 60-year-old woman with an oval, ill-defined mass in the retromamillary region. Equivalent
presentation of the mass in subtraction image of MRI using 5 ml CM (initial signal increase: 131%) (a), and a few days later with body-weighted dosage (initial signal
increase: 130%) (9 ml; 90 kg BW)(b). Histology: NOS 8 mm grade 2 pN0.
Fig. 7. a-c: Interindividual comparison of images using different matrices: left fig. 256 × 256, mid fig. 512 × 512, right fig. 1.024 × 1.024.
been used since 10 years, and CEBCT is in the status of clinical testing. possible with contrast material that allows the visualization of
Study results show that all these methods are clearly better than all not- angiogenesis.
contrast-enhanced techniques [16–20]. CE MRI of the breast is, how All depictable breast cancers are visible on MRI (angiogenesis; vital
ever, superior to all other diagnostic methods. In studies reporting a tissue) and/or on mammography (calcification; necrotic tissue).
superiority of CEM over MRI, MRI image quality was poor and inade The combination of MRI and one-view MLO MX is the so-called
quate [21]. In this paper the performance of state-of-the-art HR Breast Goettinger Optipack.
MRI will be reported on the base of 40-years of experience with this
method.
2. Hardware
The development of new diagnostic techniques in breast imaging
should not have the goal of being better than mammography. Quality assured HR MRI of the breast requires a field strength of 1.5 T
Instead the objective should be to have a sensitivity of more than or 3.0 T, a dedicated and comfortable bilateral open breast surface coil,
95% for the detection of breast carcinoma in all density types. and a dedicated MR-compatible compression device (Figs. 2, 3). A head
The depiction of microcalcifications is the domain of mammog holder with integrated mirror, a motive card, and a headset with music
raphy and mammography-based techniques, like breast CT. Calci option increase the comfort aspect and decrease the risk of disturbing
fications in breast cancer correspond to necrotic tumor tissue. It is, motion artifacts.
however, much more important to detect vital tissue. This is only
4
Fig. 8. a-e: HR Breast MRI. Trifocal breast cancer.73-year-old asymptomatic woman. Mammography density type C. Three lesions in the left breast. MIP (a),
single slice zooms with 7 mm lesion (b), 5 mm lesion (c), and 3 mm lesion (d). BCT after MR-guided localization with 3 wires. The index tumor was clip-marked after
biopsy (e). Histology: NOS, pT1b multicentric, G2.
3. Positioning in a relaxed position, e.g. in the belt of the dressing gown (Fig. 4). Plane
paddles are superior to curved paddles which may show disturbing
MRI is typically performed with the patient in a prone position, and partial volume artifacts (Fig. 3).
the breast hanging and immobilized using a dedicated compression tool
within the coil. It is usually better to position both arms along the body
5
Fig. 9. a-c: MIO Breast MRI. Breast cancer patient with suspicious focus in the contralateral breast. 69-year-old patient. BIRADS 6 left breast. Local MRI
staging with depiction of the histologically verified cancer plus EIC in the left breast. Highly suspicious focus in the contralateral breast, arrow, MR BIRADS 4 (a). T1
precontrast (b) and single slice subtraction image (c) of the right breast. No histology of the focus was obtained due to the neoadjuvant treatment concept.
Fig. 10. a,b: MIO Breast MRI. Small tumor relapse. 67-year-old patient. BCT of the left breast 10 years ago. In the current examination a small enhancing lesion is
seen in the left breast, close to the chest wall. T1 precontrast (a) and single slice subtraction image, arrow (b). Histology: Tumor relapse, NOS G2.
6
Fig. 11. MIO Breast MRI. Contralateral DCIS in staging MRI. 53-year-old patient. BIRADS 6 left breast (invasive NOS with EIC). Segmental non-mass
enhancement in the right breast, arrows. Histology: DCIS, G1.
Fig. 12. k-space and contrast encoding. First and second T1 imaging after CM with contrast encoding space in the middle of the k-space. Consecutive uptake of the
contrast information one and three minutes after application of CM.
Maximum lying-comfort on the table is the most relevant aspect of examination. After CM application an additional injection of at least 20
quality assurance in breast MRI ml of saline solution must be administered to ensure that the CM reaches
the left atrium, favorably per injector. The flow rate of CM application is
typically 3 ml/s, reduced to 2 ml /s in persons with small or vulnerable
4. Contrast material
veins.
Breast MRI requires a Gd-based CM to visualize tumor angiogenesis.
5. Spatial resolution
With respect to the first pass technique, there is no physiological reason
to choose a dosage that is adapted to the body weight. The time it takes
Early breast MRI protocols recommended the use of 256 × 256
for CM to flow from the vein in the arm via lung circulation to the breast-
matrices, depending on the power of the hardware and the capacity of
feeding arteries is nearly independent of the body weight. In this
the employed data compressor. In the 1990′s the spatial resolution of
context, the ejection fraction of the heart and hormonal status have a
breast MRI images improved by using a matrix of 512 × 512 and was
higher influence on the CM uptake in the breast than the BW. Based on
designated HR-MRI of the breast (Fig. 7a-c). Typically a field-of-view
our experience, a defined dosage of 5 ml CM (i.e. Gadobutrol ®; Gd-
between 320–360 mm is used, resulting in an in-plane-resolution of <
DO3A-butrol; 1 M; Bayer, Leverkusen, Germany) is sufficient for
1 mm × 1 mm. Slice-thickness remains between 2 and 3 mm. At present,
breast MRI studies (Fig. 5a,b; Fig. 6a,b). This amount of CM allows a
matrices of 672 × 672 are used at our institution for routine breast MRI
short and concentrated CM bolus application for the breast MRI
examinations (Fig. 8a-e), and we collected initial results using an even
7
Fig. 13. a,b: Breast MRI with CM delay 25 s. Diagnostic MRI of the breast. MIP of early subtraction images (MIP SUB1) with very strong physiological
enhancement of the parenchymal tissue (MR density/BPE type IV)(a). Repetition 4 weeks later with a modified protocol: Application of CM 25 s after starting the first
post CM sequence. MIP SUB1 with high transparency (MR density/BPE type I)(b).
Fig. 14. a-d: Density types in breast MRI after CM (BPE). Categorization of the background parenchymal enhancement BPE after CM: No enhancement, density
type I (a). Mild enhancement, density type II (b). Moderate enhancement, density type III (c). Strong enhancement, density type IV (d). Benchmark: SUB2. [22].
Fig. 15. a,b: FGT versus BPE. Intraindividual comparison.Fibroglandular tissue FGT type IV (equivalent to mammographic density type IV, extremely dense)(a)
and corresponding background parenchymal enhancement BPE in MIP SUB1 after CM (b).
greater matrix of 1.024 × 1.024, resulting in an image with more than Histologically verified DCIS in MRI using different matrices from
1.000.000 pixels (MIO Breast MRI) (Fig. 9a-c; Fig. 10a,b; Fig. 11). The 256 × 256 (a) via 512 × 512 (b) to MIO Breast MRI with 1.024 × 1.024
acquisition time per sequence using this matrix is approx. 2:30 min. pixel (c).
8
Fig. 16. Modified First Pass protocol, Breast Care Center, Göttingen. First sequence: IR T2 FS 50 slices of 2.0 mm to 2.5 mm. Following sequences: GRE T1 50
slices of 2.0 mm to 2.5 mm (equivalent to T2 in thickness and positioning) once before and twice after CM (5 ml Gadobutrol® + 20 ml saline solution, flow 3 ml/s).
Postprocessing includes subtraction of post- and pre-contrast T1 images (SUB1, SUB2) and the calculation of MIP of these subtraction images (MIP SUB1, MIP SUB2).
Finally, a MIP of FS T2 images is also calculated (MIP T2).
Fig. 17. Breast cancer size depending on MRI interval. Size of invasive breast carcinoma in dependence upon the interval between the MRI at the time of
diagnosis and the previous MRI. Encoding of tumor type (shape) and grading (color). Cut line at 12 mm (dashed red line). Millimeter league surrounded with oval
yellow-filled area. In this study 8.975 Breast MRI’s were performed in 2.333 women with an inconspicuous MRI of the breast upon initial examination. The 6.642
subsequent routine breast MRI exams were performed within an interval of no more than 2 years [37].
HR breast MRI allows a subtle morphologic evaluation of very small 6. Temporal resolution
lesions, including foci
If incremental signal resources is available in the MR equipment The maximum of CM uptake in breast cancer is 3 min after
used, they should be preferably invested in increasing the spatial peripheral-venous application of CM if there are no relevant deficits in
resolution instead of the temporal resolution blood circulation. Consequently, two T1 w sequences should be per
formed within the first 4 to 5 min after application of CM. A maximum of
90 s per sequence performance is recommended. In our own experience,
9
Fig. 18. a-c: Natural history of DCIS visualized by breast MRI. 68-year-old patient. Single-slice subtraction image of the left breast, normal findings in the initial
MRI exam (a). Discreet linear enhancement in the inner lower quadrant of the left breast, representing early tumor-neoangiogenesis 1 year later, arrow (b). Dendritic
enhancement correlating to an intraductal carcinoma another 12 months later, arrow (c). Histology: DCIS grading 2.
Fig. 19. a-c: Natural history of invasive breast cancer visualized by breast MRI. 74-year-old patient. Single-slice subtraction image of the left breast, normal
finding (a). Discrete Non-mass in the center of the left breast, representing early tumor-neoangiogenesis 14 months later (b). Small focus within the punctate
enhancement correlating to a tiny invasive carcinoma another 12 months later (c). Histology: NOS pT1a, 3 mm grading 2, pN0.
Fig. 20. ILC with high pT-score in spite of low tumor cell mass. 67-year-old asymptomatic woman. 6 mm mass in the center of the left breast. Linear-dendritic
non-mass-lesion between the index tumor and the nipple. Bifocal MR-guided vacuum biopsy revealed invasive lobular carcinoma at both locations. Mastectomy was
performed. Final diagnosis: ILC pT3 (48 mm × 42 mm × 25 mm), grading 1.
however, a time span of up to 2 to 2.5 min is acceptable. For example: If the examination is performed in an unfavorable menstrual cycle phase),
the encoding of contrast is positioned in the middle of the k-space in a 2 a delay of 20–25 s before CM application can be helpful (Fig. 13a,b).
min sequence, contrast will be highest 1 and 3 min after application of According to our experience and in analogy to breast density in
CM (Fig. 12). In this way, a suspicious uptake of CM in the tumor matrix mammography, the MR “density” type after CM (BPE) has an influence
will be reliably demonstrable and a higher resolution would only be on the reliability of finding relevant enhancing lesions in the MRI ex
required for assessing the enhancement curve type. In our clinical amination. We thus recommend to grade BPE should be described in the
experience, best diagnostic results are achieved by maximizing the report (Fig. 14a-d). In contrast, the description of the amount of fibro
spatial rather than the temporal resolution. glandular tissue (FGT) does not provide diagnostically relevant infor
Usually, the CM is applied in the time interval between the T1 pre- mation. Moreover, MRI provides additional information particularly in
contrast and the first T1 post-contrast sequence. In all cases, however, ACR breast density types C and D (Fig. 15a,b).
when a strong disturbing hormonal influence to the breast vasculariza As breast cancer has the maximum of CM uptake about 3 min after
tion can be expected (e.g. as seen in a former breast MRI exam, or in case CM application, measurements starting later than 6 min after CM
10
Fig. 21. a,b: Dramatic size increase of a G3-

carcinoma within 18 months. 55-year-old
asymptomatic woman. Single-slice subtraction
image of the initial MRI exam shows normal find
ings with foci in both breasts. Categorization: MR-
BIRADS right breast 1 / MR-BIRADS left breast 1
(a). In the single-slice subtraction image of the
following MRI exam 16 months later there is an 18
mm enhancing mass in the lower inner quadrant of
the left breast and a focus in the right breast. Cate
gorization: MR-BIRADS right breast 1 / MR-BIRADS
left breast 5. US-guided core biopsy: NOS. Final
histology: Invasive ductal carcinoma, pT1c (18
mm), grading 3, pN0, ER+, PR+, HER2neu
negative.
Table 1
Classification of motion artifacts in Breast MRI.
MR-artifact type Extent of artifact Limitation for the detection of
I no no limitations
II 1 mm − 2 mm DCIS
III 2 mm − 4 mm < pT1b
IV > 4 mm < pT2
Categorization of motion artifacts in breast MRI in 4 classes and consecutive limitations for the detection of cancer. Modified version from [22].
application are of no diagnostic benefit. As parenchymal enhancement included the dynamic T1 – sequences once before and twice after CM
continues to increase over time and many carcinomas show a wash out application. This shortened the time required for a complete examina
after the enhancement maximum, the detection of malignant tumors tion to a measurement time of 4:35 min using established sequences.
becomes harder or even impossible from minute to minute after the peak The evaluation of this First Pass technique in a clinical study showed
of breast tumor CM uptake has been reached. In contrast to some initial that a shortened protocol – study terminus was “abbreviated protocol” =
reports, we do not encounter breast carcinomas presenting with delayed ABB-MRI – was diagnostically equivalent to previous MRI modalities
enhancement only [23]. with measurement times of 15 min or more [25]. Finally, ABB-MRI
Considering this information and our decades of experience, we could be shown to be more cost-effective than the full protocol MRIs
designed a new breast MRI protocol. The idea of a “First Pass” protocol [26] and superior to all non-MRI imaging modalities, including tomo
for breast MRI was born in 2012 [24]. This first pass MRI protocol synthesis [7,27]. Other working groups modified the First-Pass
Fig. 22. a,b: Motion correction algorithm in Breast MRI. Single slice subtraction with motion artifact type II and a questionable lesion (a). Reduction of artifacts
with the MoCo algorithm and clear presentation of a spiculated small mass (b). Histology: NOS, pT1b grading 1 pN0. Software: Siemens, Erlangen.
11
Fig. 23. a,b: Motion correction algorithm in Breast MRI. Single slice subtraction with motion artifact type II. No suspicion lesion (a). Elimination of artifacts with
MoCo algorithm and clear presentation of a focus with associated NML (b). Histology: NOS, pT1a + EIC, grading 2, pN0. Software: Siemens, Erlangen.
Fig. 24. Breast imaging: The dual way. MX is recommended in women with density type ACR I and II (ACR a + b). MRI is the method of choice in women with
density type ACR III and IV (ACR c + d).
protocols, e.g. by adding T2 sequences, DWI or other measurements claustrophobia will stop the exam before CM is given.
[28–29]. Mann et al. reported 2014 on ultrafast view-sharing sequences In our institute the T2 sequence is acquired in FS-IR technique. This
for ultrafast dynamic imaging of the whole-breast [30]. allows the calculation of a T2-MIP (Fig. 16). Subtraction images were
The modified First Pass protocol that we use at our institute with a calculated from both, the first (SUB1) and the second (SUB2) post CM
frequency of approx. 20 exams / day is presented in Fig. 16. A T2 sequences. A MIP was also calculated from these images (MIP SUB1; MIP
sequence with a measurement time of about 3 min is performed before SUB2)(Fig. 16). For better comparison, we choose to perform the T2
initiation of the ABB-MRI to provide the additional T2 information, but images in the same slice thickness and position as used for the T1
foremost to allow the patient a few minutes to relax before the CE dy imaging.
namic T1wi sequences start. In our experience, anxiety decreases within
this time interval and the frequency of disturbing artifacts is reduced.
Moreover, the very small group of patients who suffer from severe
12
Fig. 25. a-c: Small breast cancer in an extremely dense breast. 46-year-old asymptomatic woman. Screening. CC projection mammography of both breasts
without any findings, density type ACR IV, MX-BIRADS 1 (a). MRI depicts a 6 mm round mass with spiculated borders in the MIP (b). Zoom magnification of single
subtraction image (c). Histology after MR-guided biopsy: NOS, B5b. Final result: IDC pT1b grading 2 pN0.
7. Evaluation criteria Dynamic criteria are used to evaluate the signal-to-time curves of
endotumoral CM uptake. In early breast MRI examinations suffering
CE MRI of the breast allows the analysis of both morphologic as well from low spatial resolution, dynamic criteria were important to assess
as perfusion aspects. Morphologic descriptors and criteria of lesions seen the probability of a lesion being malignant, and compensated in part for
on MRI are equivalent to those used for the lesion analysis in other the limited depiction of the morphology. Scoring systems were defined
imaging modalities, like MX and US. They mainly consider mass shape to provide an objective estimate of a given lesioń s likelihood of malig
and margins. The term “non-mass“ like lesion was created for non-space nancy and help to assign a BI-RADS category. The first such scoring
occupying enhancing lesions, and usually correlated with intraductal system was introduced by Fischer et al. in 1993 and includes five
proliferations, inflammatory changes, diffuse lobular carcinoma, ade empirically defined morphologic and dynamic criteria [32]. This so-
nosis, and other normal findings. The term “focus” was inaugurated to called FISCHER (or sometimes referred to as Göttingen) Score was
describe small enhancing lesions < 5 mm [31]. evaluated by several working groups and modified by other authors by
13
Fig. 26. a-c: Postoperative scar. 58-year-old patient. BCT of the right breast 3y ago. MLO projection mammography with architectural distortion and macro
calcifications, density type ACR II. MX-BIRADS 2 (a). MRI T1 image before CM shows architectural distortion (b) without any enhancement after CM, subtraction
image, MR-BIRADS 2 (c). Diagnosis: Postoperative scar.
adding information given from T2 sequences or diffusion weighted im previously used scoring systems, like FISCHER’s Goettingen Score or the
aging (DWI) [33–34]. Later, Dietzel and Baltzer created the KAISER KAISER Score, less important. An update, however, could improve the
score based on a machine-learning derived flowchart on the base of value of such scoring systems, especially for beginners.
dynamic, morphologic and T2-imaging derived criteria and named after The most important criteria leading to the detection of very small
breast MRI pioneer Werner Alois Kaiser [35]. and early breast cancers, however, are the increase of lesion’s size and
In the last 20 years, with increasing spatial resolution, the evaluation the depiction of new lesions in follow up MR imaging. Consecutive
of dynamic aspects, such as the analysis of signal-to-time curves, has breast MRI examinations in intervals of 1 to 2 years allow the detection
according to our experience, largely lost its diagnostic value. More than of invasive breast carcinomas with an average size of 5.5 mm to 12.5
ever, the current Maxime of lesion evaluation is morphology, mm, depending on the grading (G1 7.3 mm, G2 8.6 mm, G3 10.9 mm)
morphology, and morphology again. We therefore consider the value of and the tumor type (TC 5.5 mm, NOS 8.7 mm, ILC 12.5 mm)(Figs. 17
14
Fig. 27. a-c: MRI in woman with high risk profile. 52-year-old woman with a defined high risk profile. Screening. MIP with 6 mm triple negative breast cancer,
NOS p1b with EIC, grading 3.
18a–c, 19a–c). Thus, compared to all other imaging modalities, the mm. The rate of nodal negative carcinomas was 95.9%. The rate of in
diagnostic performance of consecutive breast MRI examinations at these terval carcinomas was < 2% [37].
intervals provides superior results and therefore is the “champion” in the The size of the detected invasive breast carcinomas ranged from 2 to
“millimeter league” [37]. 22 mm. The majority of tumors with a size greater than 15 mm was
Fischer et al. performed a study including 8.975 MRI’s of the breast lobular tumors. This is due to the indian-file growth pattern of lobular
in 2.333 women and patients with an inconspicuous initial examination breast cancers, resulting in large tumor sizes with a low count of tumor
(MR-BIRADS 1,2,3). Subsequent routine breast MRI examinations cells, in contrast to the solid growth pattern of ductal carcinomas
(6.642 exams = 2,85 follow-up MRI / woman) were performed within (Fig. 20). In this context, it can be debated as to whether or not the
an interval of no more than 2 years. Within the study frame, 299 sus measurement of a tumor in millimeters is an optimal criterion in staging
picious lesions categorized as BIRADS 4 or 5 were found and clarified by of invasive lobular carcinomas. There are, however, also NOS tumors
percutaneous biopsy (4.4% per round). Histology revealed benign that reach the size of 15 mm or more within an interval of 1–2 years. In
findings (B1, B2) in 158/297 (53,2%) of the cases, lesions with unclear the presented study, all of the detected invasive ductal carcinomas of 15
biological potential (B3) in 24 patients (8,1%), and malignant tumors mm or larger were tumors of grading 3 (Fig. 21a,b). On the whole,
(B5a, B5b) in 115 women (38,7%). Open biopsy of lesions with malig however, the detection of breast cancer at a stage of pT2 or higher is rare
nant results after percutaneous biopsy revealed intraductal carcinoma in if MRI is performed at intervals of 24 months or less. Based on all follow
36/115 cases (G1: 11, G2: 17, G3: 8), and an invasive breast cancer in up MRI examinations within intervals of maximum 2 years, the rate of
79/115 cases. Tumor stages were pT1a (17/79; 21,5%), pT1b (39/79, early detected carcinoma (pTis, pT1a, pT1b) was 80% [37].
49,4%), and pT1c (19/79; 24,1%). Only 5.0% (n = 4) of all cases were
classified as stage pT2. The average size of all invasive tumors was 9.0
15
Fig. 28. a,b: CUP syndrome with small index carcinoma in the right breast. 70-year-old patient. Histologically verified lymph node metastases in the right
axillary region. MLO projection mammography without suspicious lesion, density type ACR II. MX-BIRADS 1 (a). MRI shows a focus with ring enhancement in the
center of the right breast (arrow) and an enlarged axillary lymph node in the right axilla, MIP (b). Histology of the focus revealed NOS, pT1a, grading 3, pN3a.
Research dealing with an increase of diagnostic accuracy of breast 8. Diffusion weighted imaging, DWI
MRI should preferentially target sub centimeter lesions in the
“millimeter league”. Regrettably, many current publications that The implementation of DWI in MRI protocols of the breast has been
report on populations with larger masses. Diagnostic problems in the subject of research for many years [36,38–40]. At present, the
this size league are usually solvable with US of which the diagnostic following facts can be stated as an agreement between different working
results are usually not reported. groups:
16
Fig. 29. a,b: MR-monitoring of neoadjuvant therapy. 46-year-old woman with triple negative NOS grading 3 before starting neoadjuvant chemotherapy. MRI
with typical G3 - breast cancer displaying a small rim sign and central enhancement (a). Follow-up-MRI after finishing neoadjuvant therapy with complete remission
of tumor enhancement (MRI full responder)(b).
Multiple different DWI techniques are used. To homogenize pro Motion artifacts are classified into 4 categories: artifact type I to IV
tocols, an international working group recommends EPI-DWI sequences, (Table 1). Artifact type I and II are suitable for evaluation, while type III
preferably SPAIR fat suppression, TR ≥ 3000 ms, two different diffusion and IV artifacts are not. According to our experience, intravenous pre
weightings with a low b-value varying from 0 to 50 s/mm2 and a high b- medication with anxiolytic drugs may be helpful to avoid motion artifacts
value of 800 s/mm2. The quantitative Apparent Diffusion Coefficient in particularly nervous patient. If motion artifacts are, however, present in
(ADC) map is then calculated from these sequences automatically. New the acquired images, there are effective correction algorithms available to
techniques varying the b-values are intravoxel-incoherent motion im make the evaluation of these images possible. Such modern algorithms
aging and diffusion kutosis imaging. The clinical benefit of these reduce motion artifacts by applying an elastic 3D registration of the T1-
methods is the subject of current research. weighted imaging volumes prior to computation of the subtractions
Breast cancer screening using MRI without CM and DWI shows a (MOCO). To prevent the registration algorithm from having to tackle the
sensitivity of approx. 70% for breast cancer < 10 mm (millimeter lea maximum degree of motion or contrast change, the first post-contrast
gue), and does thus not achive comparable results to contrast-enhanced volume is typically used as reference because it has the favorable prop
MRI. Similar results are already possible using a combination of MX and erty of reflecting an intermediate state, not only in terms of temporal
US. motion, but also in terms of contrast enhancement. The pre-contrast and
Recommendations to include DWI in the standard protocol of the subsequent post-contrast series are then elastically registered and
Breast MRI are unwarranted as long as the value of this method is not morphed to best match the first post-contrast series within reasonable
defined. Until then, DWI has the status of work in progress. anatomical constraints of tissue plasticity (Fig. 22a,b, Fig. 23a,b).
9. Artifacts 10. Indications
To make the analysis of breast MRI images possible, it is essential MRI of the breast is indicated in all women with dense or extremely
that the T1 signal is exclusively due to CM. There are two methods dense breasts (ACR type C, D) in screening, assessment or after treat
currently used to eliminate the disturbing T1 signal of the fat tissue in ment of breast cancer (“Dual way” Fig. 24, Fig. 25a-c) [3–4,41–45]. If
breast MRI. The American way uses primary fat suppressed T1 se density type is ACR A or B, MRI is indicated, when mammography and or
quences. The European way uses a technique subtracting the pre- from US are limited or contraproductive, i.e.
post-contrast images. This European method is, however, very sensitive
to motion artifacts, i.e. changes in the position of the patient during the • follow up after BCT for differentiation between scar and tumor
image acquisition. Since the acquisition typically spans over several relapse (Fig. 26a-c) [46–47].
minutes, imaging may be affected by patient motion during the dynamic • screening in women with high risk profile (Fig. 27a,b) [48–49].
T1-weighted MRI, leading to false signal increases such as artificial skin • looking for a primary lesion in CUP syndrome (Fig. 28a,b) [50–51].
rims and other spurious structures in the computed subtraction images. • monitoring under neoadjuvant therapy (Fig. 29a,b) [52–53].
17
Fig. 30. a-c: Small contralateral carcinoma in local MR-staging. MX-BIRADS 5 on the right side. 79-year-old woman. Large breast carcinoma in the right breast
with secondary signs of malignancy and enlarged axillary lymph node in MLO-projection mammography, density type ACR II, MX-BIRADS right 5, left 1 (a,b). MRI
with large breast cancer and surrounding EIC in the right breast. On the left there is an additional 5 mm round mass close to the areola with ill-definded borders: MIP
(c). Zoom magnification of left lesion in single subtraction image (d). Histology after second look US and US-guided biopsy left breast: NOS, B5b. results: IDC pT1a
grading 1 pN0 (left breast). IDC + EIC pT2 grading 2 pN1a (right breast).
• preoperative local staging (Fig. 30a-c) [54]. In dense breasts, HR QA MRI is the screening method of choice. It is
• assessment in pathologic discharge of the nipple (Fig. 31a,b) [55]. first line in a stand-alone technique. MRI is no longer an adjunct to
• avoiding needle biopsy in suspicious microcalcifications seen on mammography
mammography (Fig. 32a,b) [56].
• problem solver (Fig. 33a,b) [57].
11. Interventions
Additionally, MRI is the method of choice in the evaluation of breast
The procedure of MR-guided interventions (localization, biopsy) is
implants. Special protocols are used to exclude complications of an
well established since more than 30 years. MR-compatible positioning
implant such as rotation, capsulitis, gel bleeding, and intra- and
equipment as well as clips, coils, wires, and systems for vacuum biopsy
extracapsular rupture (Table 2, Fig. 34) [58–61].
are required for such interventions (Fig. 35a,b; Fig. 36a,b; Fig. 37a-i).
MR-guided interventions are indicated when MR-BIRADS 4 or 5 lesions
have no certain corresponding mammographic or sonographic finding
18
Fig. 31. a,b: MRI in a patient with pathologic nipple discharge. 44-year-old woman with sanguinolent nipple discharge of the left breast. Mammography in CC
projection of the left breast with normal findings. No suspicious calcifications. Density type ACR D. MX BIRADS left breast: 1 (a). MRI with segmental Non-Mass
enhancement of the inner quadrant of the left breast (b). Histology after US-guided core biopsy of the inner quadrants: DCIS grading 2, B5a. Final histology after
mastectomy: DCIS pTis grading 2.
[5]. Second look or targeted ultrasound examinations should be per masses should be marked with clip or coil after biopsy. For preoperative
formed with the knowledge of the MR-lesion’s exact position, shape and MR-guided localization, the localization wire can be placed directly in
size (Fig. 38a-c, Fig. 39a-c). If US shows a corresponding lesion, but the lesion, or multiple localization wires can be placed at the relevant
histology reveals a benign result after US-guided core biopsy, a corner points of a lesion before segmentectomy or quadrantectomy, also
mismatch must be considered and additional MR-guided vacuum biopsy referred to as “bracketing” (Fig. 46a,b; Fig. 47a-d).
may be indicated (Fig. 40). According to the data in the literature, the rate of malignant findings
MR-guided percutaneous biopsy recommendations endorse the use in specimens after MR guided vacuum biopsy is about 30 – 40%. The rate
of vacuum systems for acquisition of 12 specimen (9G). In our experi of B3-lesions in specimens after MR guided vacuum biopsy is about 10%.
ence with a 9G-system, 6 specimens are usually sufficient to establish a The rate of complications is low (<1%), and accuracy is high (>98%)
diagnosis. Directed sampling of specimen is recommended for the biopsy [62–66].
of foci and masses, whereas a full rotation of the needle provides best
results in Non-mass lesions (Fig. 41a,b; Fig. 42a,b) [61]. In most cases, 12. Paradigm change
even difficult lesion localizations can be successfully accessed for MR-
guided biopsy (Fig. 43a,b,Fig. 44a,b; Fig. 45a,b). Foci and small Guidelines should be up-dated in the current era of quality-assured
19
Fig. 32. a,b: MRI in a patient with suspicious microcalcifications on mammography. 48-year-old asymptomatic woman. Mammography (zooming) with a
cluster of pleomorph microcalcifications in the center of of the left breast. Density type ACR D. MX BIRADS left breast: 4c (a). MRI with normal findings. No
enhancement in the area of the calcifications (b). Histology after stereotactic vacuum biopsy: regressive changed fibroadenoma. No malignancy. B2.
20
Fig. 33. a,b: MRI as a problem solver. 55-year-old woman with unclear palpable mass in the outer upper quadrant of the right breast. Mammography in CC
projection with unclear density in this area. No associated calcifications (a). MRI with normal findings. No enhancement in the area of the unclear “lesion” (b).
Diagnosis: “Pseudo”lesion (superposition of normal tissue) on mammography. Follow up without changing of the lesion greater than 2 years.
21
Table 2
Signs of increased permeability of implant shell vs. intracapsular rupture.
MRI T1 Name Diagnosis
Gel bleeding Increased permeability
Subcapsular line sign Increased permeability or intracapsular rupture
Keyhole sign, noose sign Increased permeability or intracapsular rupture
Teardrop sign Increased permeability or intracapsular rupture
Linguini sign intracapsular rupture
Ending line sign intracapsular rupture
(continued on next page)
22
Table 2 (continued )
MRI T1 Name Diagnosis
Salad oil sign intracapsular rupture
Comparison of the different signs indicating an increased implant shell permeability and an intracapsular rupture in T1 imaging [58].
Fig. 34. Extracapsular rupture of breast implant. Bilateral placement of breast implants over 25y ago. Discharge of silicone from the right implant with dis
tribution of the silicone along the ducts in direction to the nipple. Rotated, but intact left implant. Status after injection of free silicone in both retromamillary regions.
MIP of silicone-weighted, water- and fat-suppressed sequence (SILI MIP).
HR MRI of the breast, especially with respect to oncologic follow-up and HR breast MRI has excluded further ipsilateral carcinomas, adjuvant
diagnostics [67]. In our view, the indication for adjuvant radiation radiation therapy could be considered overtreatment (Fig. 48). First
therapy after BCT and management in case of tumor relapse should also steps to this topic have been published actually [68]. Moreover, as
be reviewed and revised. follow-up patients usually undergo MRI once a year after BCT, there is
Indication for adjuvant radiation therapy essentially no risk of missing a large-sized tumor relapse. In addition,
At present, adjuvant radiation therapy is usually recommended after even in the case of a relapse, long-time survival will unlikely be affected.
BCT of an invasive breast cancer or large DCIS. The goal of radiation is Proceeding in case of tumor relapse
the reduction of in-breast relapses. In contrast to mammography, how In the case of a tumor relapse or ipsilateral metachronous second
ever, modern MRI can exclude additional breast cancer manifestations breast cancer after BCT and adjuvant radiation therapy, mastectomy is
at the time of the initial diagnosis with a high reliability according to our usually recommended to patients. This is recommended because a breast
experience. Thus, when a small index lesion has been detected, and QA cannot normally be irradiated a second time with the necessary dosage.
23
Fig. 35. a,b: Tools for MR guided Interventions.Commonly used tools for MR guided biopsy and localization: Post-and-Pilar system with an interventional
carriage having a sliding in x- and y-axis (a). Grid-System with integrated perforated cubes (b). Equipment: Noras Company, Höchberg, Germany.
Fig. 36. a,b: Principle of vacuum biopsy needle. Typical examples of vacuum needle biopsy systems with specimen cutter rotating inside (a), or outside (b).
Cutter hatched.
24
Fig. 37. A-i: configuration of different types of localization wires.Large-curved J-shaped wire (Homer), easily retractable for repositioning: Constellation with
wire in the needle (a), and after removal of the needle (b). Small-curved J-shaped wire, easily retractable for repositioning: constellation with wire in the needle (c).
Palm-leaf like configuration, retractable when positioned within the needle (d, e). Wire with single hook (Hook; f, g), wire with double hooks (Double Hook; h), and
x-configurated hook wire (i). All hook wires are not retractable and can only be removed operatively.
Fig. 38. a-c: Second Look / Targeted US in MR BIRADS 4 or 5. 62-year-old woman. Screening. MRI reveals a suspicious focus in the inner lower quadrant of the
right breast (a). Potentially corresponding finding in targeted US (b). US-guided core biopsy of the lesion (c). Histology: Invasive lobular carcinoma, ILC, B5b. Final
diagnosis ILC pT1a pN0 grading 2.
25
Fig. 39. a-c: US in MR BIRADS 4 or 5. MR check after wire placement. 76-year-old woman. Screening. MRI reveals a suspicious NML in the center of the left
breast (a). Presumedly corresponding finding in US (b). US-guided core biopsy of the lesion with subsequent wire placement in the biopsy region to prove correlation
between MRI and US lesions, arrows (c). Histology: Invasive lobular carcinoma, ILC, B5b. Final diagnosis ILC pT1c pN0 grading 1.
26
Fig. 40. MR-guided vacuum biopsy. Typical prone position of the patient with fixation of the left breast in the dedicated biopsy coil with a post-and-pilar system.
Situation after placement of the coaxial and the vacuum biopsy needle. Equipment: ATEC from Hologic, Kempen, Germany.
Fig. 42. a,b: Rotating biopsy procedure. Suspicious NML in MRI (a). Posi
tioning of the vacuum biopsy needle in the center of the NML and consecutive
extraction of the specimens in a rotating manner (red arrow)(b).
Fig. 41. a,b: Unidirectional biopsy.Suspicious focus in MRI (a). Positioning

of the vacuum biopsy needle underneath the focus and consecutive unidirec
tional extraction of the specimens (red arrow)(b).
Because QA HR breast MRI can exclude additional breast cancers at the

● Sequence time about 2 min, measurement time after CM > 4 min.
time of a relapse, however, a new solitary cancer after BCT can be
● In plane resolution < 1 mm × < 1 mm, slice thickness 2 – 2.5 mm.
treated with a renewed lump- or segmentectomy (Fig. 49).
● Image subtraction SUB1 and SUB2, MIP SUB1 and MIP SUB2,
MIP T2.
Checklist of modern MRI of the breast
● Report: BPE, MRI artifact score, description of findings, MR
● MRI 1.5 T or 3.0 T. BIRADS 1–5.
● Bilateral open breast surface coil.
● Bilateral compression device.
● T2 sequence for T2 information and patient’s comfort, exam time CRediT authorship contribution statement
approx. 3–4 min.
● T1 GRE sequences once before and twice after 5 ml CM and 20 ml Uwe Fischer: Conceptualization, Data curation, Formal analysis,
NaCl. Methodology, Project administration, Resources, Visualization, Writing
27
Fig. 43. a,b: MR-guided biopsy with target lesion close to sternum. Suspicious lesion in the inner quadrant close to the chest wall (a). Documentation after
positioning the biopsy needle and removal of the specimen (b).
Fig. 44. a,b: MR-guided biopsy with target lesion close to pectoral muscle. Suspicious lesion close to the chest wall (a). Documentation after positioning the
biopsy needle and before removal of the specimen (b).
28
Fig. 45. a,b: MR-guided biopsy with target lesion close to implant. Suspicious lesion close to the capsule of an implant (a). Documentation after positioning the
biopsy needle and before removal of the specimen (b).
Fig. 46. a,b: Direct preoperative MRI-guided wire localization. NML in the right breast (a). Documentation after positioning of one wire in the center of the
lesion (b).
29
Fig. 47. a-d: Preoperative MRI-guided localization of relevant lesion borders (2wires). Suspicious dendritic NML in the left breast in MRI (a). Documentation of
the position of one wire above (b) and the second wire underneath (c) the target volume to be removed. Powerpoint with photo documentation of breast, wires, and
borders of planned segmentectomy (d).
30
Fig. 48. Sole small breast cancer in QA HR MRI of the breast. 71-year-old woman. 5 mm round mass with irregular border in the right breast, histologically
verified as NOS G2. No other ipsilateral findings. BCT after wire localization: IDC pT1a pN0 G2 R0. Is adjuvant radiation therapy of the right breast really indicated?
See [68].
Fig. 49. Metachronous breast cancer after bilateral BCT. 73-year-old patient. Bilateral BCT 12 years ago treated with adjuvant radiation therapy. Follow up MRI
was performed every 1.5 to 2 years. New 7 mm mass in the retromamillary region of the right breast. A second BCT without renewed radiation therapy seems to be a
reasonable therapeutic option. Follow up MRI once a year.
- original draft. enhanced magnetic resonance imaging (high breast cancer risk Italian 1 study),
Final Results. Invest Radiol 46 (2011) 94–105.
[5] Interdisziplinäre S3-Leitlinie für die Früherkennung, Diagnostik, Therapie und
Declaration of Competing Interest Nachsorge des Mammakarzinoms, Februar 2020.
[6] P. Skaane, A.I. Bandos, R. Gullien, E.B. Eben, U. Ekseth, U. Haakenaasen, M. Izadi,
I.N. Jebsen, G. Jahr, M. Krager, L.T. Niklason, S. Hofvind, D. Gur, Comparison of
The authors declare that they have no known competing financial
digital mammography alone and digital mammography plus tomosynthesis in a
interests or personal relationships that could have appeared to influence population-based screening program, Radiology 267 (1) (2013) 47–56.
the work reported in this paper. [7] C.E. Comstock, C. Gatsonis, G.M. Newstead, B.S. Snyder, I.F. Gareen, J.T. Bergin,
H. Rahbar, J.S. Sung, C. Jacobs, J.A. Harvey, M.H. Nicholson, R.C. Ward, J. Holt,
A. Prather, K.D. Miller, M.D. Schnall, C.K. Kuhl, Comparison of abbreviated breast
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European Journal of Radiology 167 (2023) 111053

Contents lists available at ScienceDirect

European Journal of Radiology

Breast MRI – The champion in the millimeter league

1. Introduction nodes (<5%), thus staged as pN0.

Fig. 21. a,b: Dramatic size increase of a G3-

9. Artifacts 10. Indications

Gel bleeding Increased permeability

Subcapsular line sign Increased permeability or intracapsular rupture

Keyhole sign, noose sign Increased permeability or intracapsular rupture

Teardrop sign Increased permeability or intracapsular rupture

Linguini sign intracapsular rupture

Ending line sign intracapsular rupture

(continued on next page)

Salad oil sign intracapsular rupture

Fig. 41. a,b: Unidirectional biopsy.Suspicious focus in MRI (a). Positioning

Because QA HR breast MRI can exclude additional breast cancers at the

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