Abstract

Breast MRI offers high sensitivity for breast cancer detection, with preferential detection of high-grade invasive cancers when compared to mammography and ultrasound. Despite the clear benefits of breast MRI in cancer screening, its cost, patient tolerance, and low utilization remain key issues. Abbreviated breast MRI, in which only a select number of sequences and postcontrast imaging are acquired, exploits the high sensitivity of breast MRI while reducing table time and reading time to maximize availability, patient tolerance, and accessibility. Worldwide studies of varying patient populations have demonstrated that the comparable diagnostic accuracy of abbreviated breast MRI is comparable to a full diagnostic protocol, highlighting the emerging role of abbreviated MRI screening in patients with an intermediate and high lifetime risk of breast cancer. The purpose of this review is to summarize the background and current literature relating to abbreviated MRI, highlight various protocols utilized in current multicenter clinical trials, describe workflow and clinical implementation issues, and discuss the future of abbreviated protocols, including advanced MRI techniques.

Key Messages
  • Clinical studies to date have shown that the diagnostic accuracy of abbreviated breast MRI is comparable to a full diagnostic protocol.

  • Clinical challenges to the implementation of an abbreviated breast MRI program include the lack of a Current Procedural Terminology (CPT) code for billing, optimizing turnaround time between studies, protocol standardization, and clinical interpretation time.

  • Future directions include the use of multiparametric protocols, ultrafast imaging, and the use of machine learning in image reconstruction and analysis.

Introduction

Multiple randomly assigned clinical trials have demonstrated that screening mammography reduces breast cancer mortality and allows for detection of early stage, more easily treated breast cancer (1). Mammography is the mainstay of breast cancer screening and is offered in the United States annually starting at age 40 (2) and biennially in Europe (3). However, mammography is limited in patients with dense fibroglandular breast tissue (4). Since mammography evaluates structural changes over time within the breast parenchyma, it is unsurprising that mammographically-detected cancers are more likely to be slower-growing, low-grade cancers or ductal carcinoma in situ (DCIS) that gradually produce changes in the breast parenchyma (5, 6). Conversely, more biologically relevant, higher-stage cancers are often indistinguishable from or masked by benign breast tissue on mammography (5, 6).

Breast MRI offers two inherent advantages over screening mammography in cancer detection: the superior tissue contrast offered by MRI and the physiologic uptake of gadolinium contrast. As cancers promote angiogenesis, the rapid wash-in and wash-out of contrast observed in most cancers allows for both functional and morphologic evaluation of breast lesions. The combination of soft tissue contrast and gadolinium uptake explains the high sensitivity of breast MRI when compared to other screening modalities (7–10) and the preferential detection of high-grade invasive cancers on breast MRI compared to mammography and ultrasound (6).

Due to the high cost and limited availability of breast MRI, it has traditionally been offered to those patients considered at high (>20%) lifetime risk of breast cancer (11). The prospective, multi-institutional Evaluation of Imaging Methods for Secondary Prevention of Familial Breast Cancer (EVA) trial, conducted on 687 patients at increased risk of breast cancer, demonstrated that adding supplemental breast MRI screening had a cancer detection rate of 16.0 per 1000 women when combined with screening mammography, compared to 7.7 per 1000 women when compared to mammography and ultrasound screening alone (9). The American College of Radiology Imaging Network (ACRIN) 6666 study similarly demonstrated the high sensitivity and cost-effectiveness for breast MRI compared to screening mammography and ultrasound in a high-risk population, with an additional cancer detection rate of 14.7 per 1000 women in 612 women who underwent breast MRI after 3 rounds of screening with mammography and ultrasound (8). Importantly, ACRIN 6666 also demonstrated the underutilization of MRI: even when these patients were offered a free breast MRI as part of the clinical trial, only 57.9% of patients participated (12). Despite clinical and patient education since these trials, a recent analysis of breast MRI utilization demonstrated that only 1.5% of women with high lifetime risk have ever had a breast MRI (13).

Further studies have shown that women at intermediate lifetime risk (15%–20%) of breast cancer can similarly benefit from breast MRI (10, 11). The increased cancer detection rate with breast MRI can also be seen in women at average risk; a recent study by Kuhl et al demonstrated a cancer detection rate of 15.5 per 1000 women with no interval cancers detected, suggesting that women at average risk may benefit even if screened every 2 to 3 years with MRI (14).

Despite the clear benefits of breast MRI in cancer screening, cost, patient tolerance of the exam, and accessibility remain key issues. A growing number of women at increased risk of breast cancer who might benefit from breast MRI have high deductible insurance plans (15) for which an MRI copay may be a prohibitive expense. The prone positioning traditionally used for breast MRI is difficult for many women to tolerate, leading to motion degradation and patient reluctance to undergo future breast MRI. Finally, socioeconomic disparities have been observed in screening breast MRI, with nonurban residents traveling longer to obtain it (16). Abbreviated breast MRI, in which only a select number of sequences and postcontrast imaging are acquired, exploits the high sensitivity of breast MRI while reducing table time and reading time to maximize availability and improve patient tolerance and accessibility of breast MRI. First described in 2014 by Kuhl et al (14), abbreviated breast MRI has rapidly become integrated into many practices and academic institutions. As the first prospective multicenter clinical trial comparing abbreviated MRI to digital breast tomosynthesis (DBT) has recently released initial results (17), increased use of this screening methodology is anticipated worldwide.

Therefore, the purpose of this article is to summarize the current literature relating to abbreviated MRI, to describe current multicenter clinical trials, to discuss the role of an abbreviated MRI in the setting of high-risk screening and other potential clinical indications, to highlight workflow and implementation issues, and to discuss the future of abbreviated protocols including advanced MRI techniques.

Abbreviated MRI protocol

In 2014, Kuhl et al reported on the feasibility of an abbreviated MRI protocol for breast cancer screening, including a noncontrast T1-weighted and first postcontrast T1-weighted sequence, subtraction images, and a single maximum intensity projection (MIP) image (14). This abbreviated protocol was performed in 606 screening MRI in 443 women at mildly to moderately increased risk of breast cancer. This landmark study found that all 11 cancers were seen on both the abbreviated and full breast MRI protocols. Also, the authors found similar diagnostic accuracies with both protocols: specificity and positive predictive value (PPV) of abbreviated versus full diagnostic protocol were equivalent (94.3% vs. 93.9% and 24.4% vs. 23.4%, respectively). There was a substantially reduced time for image acquisition (17 minutes vs. 3 minutes) and radiologist interpretation. Average interpretation time of the abbreviated protocol was 28 seconds for the first postcontrast images and 2.8 seconds for the MIP image alone. All 11 breast cancers were identified on both protocols with equivalent diagnostic accuracy, while the interpretation of MIP images alone missed one cancer.

To summarize, the typical full breast MRI examination includes T2-weighted and T1- weighted precontrast sequences and at least three T1-weighted postcontrast sequences, with ordinary postprocessing, usually including subtraction and maximum intensity projection (MIP) images. The American College of Radiology (ACR) accreditation requirements for breast MRI include a scout localizer, a T2-weighted sequence and precontrast, and early postcontrast and delayed postcontrast T1-weighted images (10, 18). In contrast, the essential sequences for abbreviated breast MRI include only a single series of T1-weighted pre- and postcontrast imaging, usually with generated subtraction images (Figures 1–3). Multiple variations on this basic protocol have been tested in the literature; the different studies and abbreviated protocols to date are summarized in Table 1.

82-year-old woman with heterogeneously dense breasts presenting with new right breast erythema and inconclusive mammogram and ultrasound. Abbreviated MRI demonstrates a 2.5-cm irregular, heterogeneously enhancing mass (arrow) in the right breast at 12 o’clock retroareolar depth, seen on the maximum intensity projection (MIP) image (A), first postcontrast T1-weighted images (B), and corresponding subtraction images (C). There is low to intermediate T2-weighted signal (D). MR-guided biopsy yielded chronic abscess. Partially visualized axillary adenopathy was reactive at ultrasound-guided fine needle aspiration biopsy.
Figure 1.

82-year-old woman with heterogeneously dense breasts presenting with new right breast erythema and inconclusive mammogram and ultrasound. Abbreviated MRI demonstrates a 2.5-cm irregular, heterogeneously enhancing mass (arrow) in the right breast at 12 o’clock retroareolar depth, seen on the maximum intensity projection (MIP) image (A), first postcontrast T1-weighted images (B), and corresponding subtraction images (C). There is low to intermediate T2-weighted signal (D). MR-guided biopsy yielded chronic abscess. Partially visualized axillary adenopathy was reactive at ultrasound-guided fine needle aspiration biopsy.

57-year-old woman with strong family history of breast cancer and CHEK2 mutation carrier undergoing increased-risk breast cancer screening. Previous mammogram was negative. 0.7-cm irregular, homogeneously enhancing mass in the right breast at 11 o’clock (arrow) is seen on the maximum intensity projection (MIP) image (A) but better characterized on first postcontrast T1-weighted images (B) and corresponding subtraction images (C). There is no increased T2 signal (D). MRI-directed ultrasound-guided core-needle biopsy yielded intermediate grade invasive ductal carcinoma.
Figure 2.

57-year-old woman with strong family history of breast cancer and CHEK2 mutation carrier undergoing increased-risk breast cancer screening. Previous mammogram was negative. 0.7-cm irregular, homogeneously enhancing mass in the right breast at 11 o’clock (arrow) is seen on the maximum intensity projection (MIP) image (A) but better characterized on first postcontrast T1-weighted images (B) and corresponding subtraction images (C). There is no increased T2 signal (D). MRI-directed ultrasound-guided core-needle biopsy yielded intermediate grade invasive ductal carcinoma.

25-year-old woman with personal history of MUTHY mutation carrier presenting for high-risk screening prior to planned prophylactic mastectomies. In the left breast at 3 c’clock, there is 0.8-cm focal nonmass enhancement (arrow), less prominent on the maximum intensity projection (MIP) image (A) but clearly seen on first postcontrast T1-weighted images (B) and corresponding subtraction images (C). There is no T2 correlate (D). MRI-guided biopsy yielded moderate grade ductal carcinoma in situ.
Figure 3.

25-year-old woman with personal history of MUTHY mutation carrier presenting for high-risk screening prior to planned prophylactic mastectomies. In the left breast at 3 c’clock, there is 0.8-cm focal nonmass enhancement (arrow), less prominent on the maximum intensity projection (MIP) image (A) but clearly seen on first postcontrast T1-weighted images (B) and corresponding subtraction images (C). There is no T2 correlate (D). MRI-guided biopsy yielded moderate grade ductal carcinoma in situ.

Table 1.

Summary of Sequences Included in Various Abbreviated MRI Protocols

Standard Temporal Resolution
ReferenceUltrafastUnenhanced T1-weightedFirst Postcontrast T1WSecond/Delayed postcontrast T1WT2WSubtractionMIP
Platel et al 2014 (53)TWISTYYNNYY
Kuhl et al 2014 (14)NAYYNNYY
Mann et al 2014 (49)TWISTNNNNNN
Mango et al 2015 (19)NAYYNNYY
Grimm et al 2015 (20)NAYYYYYN
Harvey et al 2016 (28)NAYYNNYY
Heacock et al 2016 (22)NAYYNYYN
Moschetta et al 2016 (23)NAYYNYYY
Pineda et al 2016 (52)High spatial and temporal resolutionYYNNYY
Abe et al 2016 (47)High spatial and temporal resolutionYYNNYN
Machida et al 2017 (24)TWISTYYNNNN
Chen et al 2017 (46)NAYYNNYY
Strahle et al 2017 (36)NAYYYYYN
Petrillo et al 2017 (37)NAYYNNYY
Panigrahi et al 2017 (26)NAYYNNYY
Romeo et al 2017 (27)NAYYNYYN
Oldrini et al 2017 (33)TRICKSYYNYYN
Choi et al 2017 (34)NAYYNYYY
Dogan et al 2017 (35)NAYYNYYN
Oldrini et al 2018 (25)NAYYNNYN
Jimenez et al 2018 (50)SVIPR STELLRYYNNYY
Standard Temporal Resolution
ReferenceUltrafastUnenhanced T1-weightedFirst Postcontrast T1WSecond/Delayed postcontrast T1WT2WSubtractionMIP
Platel et al 2014 (53)TWISTYYNNYY
Kuhl et al 2014 (14)NAYYNNYY
Mann et al 2014 (49)TWISTNNNNNN
Mango et al 2015 (19)NAYYNNYY
Grimm et al 2015 (20)NAYYYYYN
Harvey et al 2016 (28)NAYYNNYY
Heacock et al 2016 (22)NAYYNYYN
Moschetta et al 2016 (23)NAYYNYYY
Pineda et al 2016 (52)High spatial and temporal resolutionYYNNYY
Abe et al 2016 (47)High spatial and temporal resolutionYYNNYN
Machida et al 2017 (24)TWISTYYNNNN
Chen et al 2017 (46)NAYYNNYY
Strahle et al 2017 (36)NAYYYYYN
Petrillo et al 2017 (37)NAYYNNYY
Panigrahi et al 2017 (26)NAYYNNYY
Romeo et al 2017 (27)NAYYNYYN
Oldrini et al 2017 (33)TRICKSYYNYYN
Choi et al 2017 (34)NAYYNYYY
Dogan et al 2017 (35)NAYYNYYN
Oldrini et al 2018 (25)NAYYNNYN
Jimenez et al 2018 (50)SVIPR STELLRYYNNYY

Sequences listed as “ultrafast” have a temporal resolution of less than 10 seconds and were run both before and after contrast injection.

Abbreviations: MIP, maximum intensity projection; N, no; NA, not applicable; STELLR, spatial compressed sensing with temporal local low-rank; SVIPR, subtracted vastly undersampled isotropic projection; T1W, T1-weighted; T2W, T2-weighted; TRICKS, time resolved imaging of contrast kinetics; TWIST, time-resolved angiography with interleaved stochastic trajectories; Y, Yes.

Table 1.

Summary of Sequences Included in Various Abbreviated MRI Protocols

Standard Temporal Resolution
ReferenceUltrafastUnenhanced T1-weightedFirst Postcontrast T1WSecond/Delayed postcontrast T1WT2WSubtractionMIP
Platel et al 2014 (53)TWISTYYNNYY
Kuhl et al 2014 (14)NAYYNNYY
Mann et al 2014 (49)TWISTNNNNNN
Mango et al 2015 (19)NAYYNNYY
Grimm et al 2015 (20)NAYYYYYN
Harvey et al 2016 (28)NAYYNNYY
Heacock et al 2016 (22)NAYYNYYN
Moschetta et al 2016 (23)NAYYNYYY
Pineda et al 2016 (52)High spatial and temporal resolutionYYNNYY
Abe et al 2016 (47)High spatial and temporal resolutionYYNNYN
Machida et al 2017 (24)TWISTYYNNNN
Chen et al 2017 (46)NAYYNNYY
Strahle et al 2017 (36)NAYYYYYN
Petrillo et al 2017 (37)NAYYNNYY
Panigrahi et al 2017 (26)NAYYNNYY
Romeo et al 2017 (27)NAYYNYYN
Oldrini et al 2017 (33)TRICKSYYNYYN
Choi et al 2017 (34)NAYYNYYY
Dogan et al 2017 (35)NAYYNYYN
Oldrini et al 2018 (25)NAYYNNYN
Jimenez et al 2018 (50)SVIPR STELLRYYNNYY
Standard Temporal Resolution
ReferenceUltrafastUnenhanced T1-weightedFirst Postcontrast T1WSecond/Delayed postcontrast T1WT2WSubtractionMIP
Platel et al 2014 (53)TWISTYYNNYY
Kuhl et al 2014 (14)NAYYNNYY
Mann et al 2014 (49)TWISTNNNNNN
Mango et al 2015 (19)NAYYNNYY
Grimm et al 2015 (20)NAYYYYYN
Harvey et al 2016 (28)NAYYNNYY
Heacock et al 2016 (22)NAYYNYYN
Moschetta et al 2016 (23)NAYYNYYY
Pineda et al 2016 (52)High spatial and temporal resolutionYYNNYY
Abe et al 2016 (47)High spatial and temporal resolutionYYNNYN
Machida et al 2017 (24)TWISTYYNNNN
Chen et al 2017 (46)NAYYNNYY
Strahle et al 2017 (36)NAYYYYYN
Petrillo et al 2017 (37)NAYYNNYY
Panigrahi et al 2017 (26)NAYYNNYY
Romeo et al 2017 (27)NAYYNYYN
Oldrini et al 2017 (33)TRICKSYYNYYN
Choi et al 2017 (34)NAYYNYYY
Dogan et al 2017 (35)NAYYNYYN
Oldrini et al 2018 (25)NAYYNNYN
Jimenez et al 2018 (50)SVIPR STELLRYYNNYY

Sequences listed as “ultrafast” have a temporal resolution of less than 10 seconds and were run both before and after contrast injection.

Abbreviations: MIP, maximum intensity projection; N, no; NA, not applicable; STELLR, spatial compressed sensing with temporal local low-rank; SVIPR, subtracted vastly undersampled isotropic projection; T1W, T1-weighted; T2W, T2-weighted; TRICKS, time resolved imaging of contrast kinetics; TWIST, time-resolved angiography with interleaved stochastic trajectories; Y, Yes.

Literature on abbreviated breast MRI

The initial findings by Kuhl et al were supported by Mango et al (19), who retrospectively analyzed 100 biopsy-proven unicentric breast cancers using an abbreviated protocol similar to Kuhl et al (14). All 100 breast cancers were found by at least one of four readers, with mean sensitivity of 96% for the first subtraction sequence and 93% for the MIP image. Mango et al concluded that the MIP image alone is insufficient for breast cancer evaluation and a review of the first postcontrast sequence is required for interpretation. Mango et al also reported substantially faster image acquisition time (10–15 minutes imaging time compared to 30–40 minutes for a full protocol) and shorter interpretation times (mean 44 seconds, range 11–167 seconds). Cancers missed by at least one radiologist were more likely to be a low-grade invasive cancer or DCIS, with axillary lesions noted as an additional potential pitfall of reviewing the MIP image alone.

Subsequent early studies have attempted to identify how many postcontrast sequences are needed in an abbreviated protocol. Grimm et al compared the performance of 2 abbreviated MRI protocols to a full protocol for breast cancer screening in 48 high-risk women (20). The abbreviated protocol included T2-weighted precontrast and first postcontrast sequences with and without second postcontrast sequences; there was no significant difference in sensitivity (86%–95%) or specificity (52%–45%) compared to the full protocol and no difference in radiologist interpretation time between the abbreviated and full protocols. Grimm et al noted that additional sequences beyond the first or second postcontrast T1-weighted images are not routinely used to make clinical assessments (21).

Given these different abbreviated MRI protocols, efforts have been made to identify the limitations of abbreviated protocols and to offset the perceived lower specificity of abbreviated breast MRI. Heacock et al evaluated 107 biopsy-proven breast cancers in an abbreviated MRI protocol, evaluating what types of cancers were likely to be missed. Abbreviated protocols included precontrast and first postcontrast T1-weighted imaging with and without T2-weighted imaging and with and without prior images. The study had a sensitivity of 97.8%–99.4% for cancer detection (22). Importantly, missed cancers were more likely to bea low-grade invasive cancer and/or DCIS, similar to that noted in Mango et al (19).

While the abbreviated protocols markedly reduced interpretation time in many studies (14, 19, 22) only one study showed no difference in interpretation time between a full and abbreviated protocol (20). It is important to note that the interpretation time is solely defined by the interpretation of the abbreviated breast MRI protocol. The interpretation time did not account for the review of mammograms, breast ultrasound, prior breast MRI exams, and correlating with the clinicopathologic information for each patient. In almost all the studies the shorter acquisition time and faster image interpretation in abbreviated protocols had no negative effect on diagnostic accuracy (14, 19, 23–28). To date, abbreviated breast MRI has been performed in over 5400 women in 8 different nations (Table 2) with similar accuracy despite varied populations. All of these findings highlight the fact that supplemental MRI screening using abbreviated protocols is well positioned to detect biologically aggressive and mammographically occult breast cancer while substantially shortening overall imaging time.

Table 2.

Summary of Abbreviated Breast MRI Studies Worldwide. To Date, Varying Protocols and Patient Populations have Nonetheless Consistently Demonstrated High Sensitivity of Abbreviated Breast MRI

ReferenceCountryStudy PopulationNo. of PatientsSensitivity (%)Specificity (%)Max AUC
Platel et al 2014 (53)The NetherlandsClinical population137NRNR0.87
Kuhl et al 2014 (14)GermanyScreening60610094.3NA
Mann et al 2014 (49)NetherlandsClinical population16090670.812
Mango et al 2015 (19)U.S. (MSKCC)Known cancer10093–98NANA
Grimm et al 2015 (20)U.S. (Duke)Enriched4886–8945–52NA
Harvey et al 2016 (28)U.S. (Johns Hopkins)High-risk screening56810094NA
Heacock et al 2016 (22)U.S. (NYU)Known cancer10797.8–99.4NANA
Moschetta et al 2016 (23)ItalyClinical population4708991NA
Abe et al 2016 (47)U.S. (Univ. Chicago)Selected cases6085790.89
Machida et al 2017 (24)JapanEnriched8887.1–93.583.4–91.7NA
Chen et al 2017 (46)ChinaDense breast screening47892.9–93.886.5–88.3NA
Petrillo et al 2017 (37)ItalyConsecutive cases50899.575.4NA
Panigrahi et al 2017 (26)U.S. (Johns Hopkins)Screening105281.897.2NA
Romeo et al 2017 (27)ItalySelected cases989993NA
Oldrini et al 2017 (33)FranceConsecutive7093.170.8–83.3NA
Choi et al 2017 (34)South KoreaAfter breast cancer72510089.2NA
Oldrini et al 2018 (25)FranceSelected cases9010095.1NA
Lee-Felker et al 2019 (55)U.S. (UCLA)Extent of disease819997NA
Summary544694.0 (81.8–100)89.8 (45–97.2)
ReferenceCountryStudy PopulationNo. of PatientsSensitivity (%)Specificity (%)Max AUC
Platel et al 2014 (53)The NetherlandsClinical population137NRNR0.87
Kuhl et al 2014 (14)GermanyScreening60610094.3NA
Mann et al 2014 (49)NetherlandsClinical population16090670.812
Mango et al 2015 (19)U.S. (MSKCC)Known cancer10093–98NANA
Grimm et al 2015 (20)U.S. (Duke)Enriched4886–8945–52NA
Harvey et al 2016 (28)U.S. (Johns Hopkins)High-risk screening56810094NA
Heacock et al 2016 (22)U.S. (NYU)Known cancer10797.8–99.4NANA
Moschetta et al 2016 (23)ItalyClinical population4708991NA
Abe et al 2016 (47)U.S. (Univ. Chicago)Selected cases6085790.89
Machida et al 2017 (24)JapanEnriched8887.1–93.583.4–91.7NA
Chen et al 2017 (46)ChinaDense breast screening47892.9–93.886.5–88.3NA
Petrillo et al 2017 (37)ItalyConsecutive cases50899.575.4NA
Panigrahi et al 2017 (26)U.S. (Johns Hopkins)Screening105281.897.2NA
Romeo et al 2017 (27)ItalySelected cases989993NA
Oldrini et al 2017 (33)FranceConsecutive7093.170.8–83.3NA
Choi et al 2017 (34)South KoreaAfter breast cancer72510089.2NA
Oldrini et al 2018 (25)FranceSelected cases9010095.1NA
Lee-Felker et al 2019 (55)U.S. (UCLA)Extent of disease819997NA
Summary544694.0 (81.8–100)89.8 (45–97.2)

Abbreviations: AUC, area under the curve; MSKCC, Memorial Sloan-Kettering Cancer Center; NA, not applicable; NR, not recorded; NYU, New York University; UCLA, University of California – Los Angeles; U.S., United States.

Table 2.

Summary of Abbreviated Breast MRI Studies Worldwide. To Date, Varying Protocols and Patient Populations have Nonetheless Consistently Demonstrated High Sensitivity of Abbreviated Breast MRI

ReferenceCountryStudy PopulationNo. of PatientsSensitivity (%)Specificity (%)Max AUC
Platel et al 2014 (53)The NetherlandsClinical population137NRNR0.87
Kuhl et al 2014 (14)GermanyScreening60610094.3NA
Mann et al 2014 (49)NetherlandsClinical population16090670.812
Mango et al 2015 (19)U.S. (MSKCC)Known cancer10093–98NANA
Grimm et al 2015 (20)U.S. (Duke)Enriched4886–8945–52NA
Harvey et al 2016 (28)U.S. (Johns Hopkins)High-risk screening56810094NA
Heacock et al 2016 (22)U.S. (NYU)Known cancer10797.8–99.4NANA
Moschetta et al 2016 (23)ItalyClinical population4708991NA
Abe et al 2016 (47)U.S. (Univ. Chicago)Selected cases6085790.89
Machida et al 2017 (24)JapanEnriched8887.1–93.583.4–91.7NA
Chen et al 2017 (46)ChinaDense breast screening47892.9–93.886.5–88.3NA
Petrillo et al 2017 (37)ItalyConsecutive cases50899.575.4NA
Panigrahi et al 2017 (26)U.S. (Johns Hopkins)Screening105281.897.2NA
Romeo et al 2017 (27)ItalySelected cases989993NA
Oldrini et al 2017 (33)FranceConsecutive7093.170.8–83.3NA
Choi et al 2017 (34)South KoreaAfter breast cancer72510089.2NA
Oldrini et al 2018 (25)FranceSelected cases9010095.1NA
Lee-Felker et al 2019 (55)U.S. (UCLA)Extent of disease819997NA
Summary544694.0 (81.8–100)89.8 (45–97.2)
ReferenceCountryStudy PopulationNo. of PatientsSensitivity (%)Specificity (%)Max AUC
Platel et al 2014 (53)The NetherlandsClinical population137NRNR0.87
Kuhl et al 2014 (14)GermanyScreening60610094.3NA
Mann et al 2014 (49)NetherlandsClinical population16090670.812
Mango et al 2015 (19)U.S. (MSKCC)Known cancer10093–98NANA
Grimm et al 2015 (20)U.S. (Duke)Enriched4886–8945–52NA
Harvey et al 2016 (28)U.S. (Johns Hopkins)High-risk screening56810094NA
Heacock et al 2016 (22)U.S. (NYU)Known cancer10797.8–99.4NANA
Moschetta et al 2016 (23)ItalyClinical population4708991NA
Abe et al 2016 (47)U.S. (Univ. Chicago)Selected cases6085790.89
Machida et al 2017 (24)JapanEnriched8887.1–93.583.4–91.7NA
Chen et al 2017 (46)ChinaDense breast screening47892.9–93.886.5–88.3NA
Petrillo et al 2017 (37)ItalyConsecutive cases50899.575.4NA
Panigrahi et al 2017 (26)U.S. (Johns Hopkins)Screening105281.897.2NA
Romeo et al 2017 (27)ItalySelected cases989993NA
Oldrini et al 2017 (33)FranceConsecutive7093.170.8–83.3NA
Choi et al 2017 (34)South KoreaAfter breast cancer72510089.2NA
Oldrini et al 2018 (25)FranceSelected cases9010095.1NA
Lee-Felker et al 2019 (55)U.S. (UCLA)Extent of disease819997NA
Summary544694.0 (81.8–100)89.8 (45–97.2)

Abbreviations: AUC, area under the curve; MSKCC, Memorial Sloan-Kettering Cancer Center; NA, not applicable; NR, not recorded; NYU, New York University; UCLA, University of California – Los Angeles; U.S., United States.

T2-weighted imaging

Given the variability in abbreviated MRI protocols, studies have attempted to determine which sequences may be the most effective. T2-weighted images have been shown to improve lesion characterization in full diagnostic MRI (29, 30). Of note, these studies were performed early in the development of breast MRI, and more recent evidence of the added value of T2-weighted sequences in breast MRI has been lacking (31, 32). However, T2 weighted imaging is considered a minimal requirement for ACR breast MRI accreditation (29), and it is perhaps because of this that multiple groups (20, 23, 33–35) have included a T2-weighted sequence in their abbreviated protocol, including the ongoing Eastern Cooperative Oncology Group-American College of Radiology Imaging (ECOG-ACRIN) 1141 comparison of abbreviated MRI and DBT. These studies do not directly evaluate the additive benefit of T2-weighted imaging.

Although Grimm et al included T2-weighted imaging in their protocol (20), they did not specifically evaluate how this changed interpretation time. In contrast, Heacock et al (22) found that the addition of T2-weighted sequences had no effect on cancer detection in a population of unifocal breast cancers but increased lesion conspicuity. The authors noted that the T2-weighted sequences added a mean of 5 to 10 seconds to interpretation time, but substantially increased the scan time by 5 minutes. However, the authors suggested that the inclusion of T2-weighted imaging may be better evaluated in the screening setting. Strahle et al subsequently used 452 lesions to prospectively identify the most important sequences for breast MRI screening (36); they concluded that T2-weighted precontrast, T1-weighted precontrast, and first and late postcontrast sequences are necessary in screening breast MRI, with a scan time of 7.5 minutes.

Research assessing the impact of T2-weighted imaging in abbreviated MR protocols is therefore limited. Some studies (14, 19, 37) demonstrating comparable diagnostic accuracy between abbreviated protocols without T2-weighted images and full diagnostic MRI protocols suggest that T2-weighted sequences may not add significant benefit. However, as few of these studies have been done in a pure screening population, it is possible that the added value of T2-weighted imaging may be most valuable in increasing specificity and biopsy PPV, similar to its use in routine breast MRI

Noncontrast abbreviated MRI

The relatively recent discovery that gadolinium accumulates in the brain of patients with normal renal function has raised concern about the safety of contrast-enhanced MRI (38). To date, there is no evidence that this gadolinium deposition causes clinical symptomatology, although the potential risks are under ongoing investigation. The FDA stated that “health care professionals should consider limiting gadolinium-based contrast agent use to clinical circumstances in which the additional information provided by the contrast is necessary,” (39) and therefore the use of gadolinium should be carefully considered before it is implemented in a large screening population. Pertinent to this scenario, a recent study of healthy women who had undergone multiple rounds of screening breast MRI demonstrated no T1 signal changes in the deep brain nuclei of these patients (40), suggesting that in this healthy population the concerns surrounding gadolinium administration may be less applicable.

Diffusion-weighted imaging (DWI) is a potential imaging biomarker that does not require gadolinium contrast. Studies evaluating noncontrast abbreviated MRI protocols with combinations of DWI, with T1-weighted and/or T2-weighted sequences, show sensitivities of 40%–78% (41–43). Note that these studies do not replicate real-world screening scenarios, as their study populations were enriched with breast cancers. Their low sensitivities suggest that for now, DWI remains an inferior technique for the detection of breast cancer.

Diffusion-weighted imaging shows more promise in characterizing lesions that have already been identified rather than detecting lesions in a screening setting. For example, in a study of patients with mammographically-detected suspicious findings recommended for biopsy, an abbreviated protocol of DWI and T2-weighted images was able to discriminate benign from malignant lesions, with a 0.92 negative predictive value and 0.93 PPV (44). A study of patients with suspicious mammographic or sonographic lesions demonstrated lower accuracy of DWI compared with DCE-MRI (83.7% vs. 90.6%) and lower sensitivity of DWI (82% vs. 100%) (45). This study showed that DWI was limited in the detection of invasive lobular carcinomas, mucinous cancers, invasive cancers presenting as diffuse nonmass enhancement, and lesions smaller than 12 mm. Further studies of DWI should include a wide range of histopathologic types of breast cancers to fully evaluate its accuracy in a real-world setting.

Multiparametric MRI

While DWI is not sufficiently sensitive to be used as a standalone sequence for breast cancer screening, adding DWI to a contrast-enhanced abbreviated protocol has the potential to improve accuracy. In a study of abbreviated protocols consisting of the first postcontrast subtracted sequence with and without the addition of DWI, the multiparametric protocol with DWI yielded higher specificity and sensitivity (46). In fact, the performance of the multiparametric abbreviated protocol was not significantly different from that of the full diagnostic MRI protocol (sensitivity of 100% for both), while the abbreviated protocol without DWI was significantly less specific (86.5% vs. 95.0% for the multiparametric protocol and 96.8% for the full protocol).

Ultrafast abbreviated breast MRI

A known drawback of abbreviated breast MRI protocols is the absence of kinetic analysis information on the wash-in and wash-out of contrast due to the omission of delayed postcontrast sequences. Instead, new ultrafast and accelerated breast MRI techniques have allowed for the analysis of the rapid wash-in of contrast at temporal resolutions of less than 10 seconds/frame. These sequences often utilize various k-space view-sharing and compressed sensing techniques where the central region of k-space is sampled continuously but the outer region is only partially sampled at different timepoints (47–50). This allows for simultaneous high temporal resolution with a minimal decrease in spatial resolution.

Ultrafast techniques can detect the rapid, early wash-in of contrast compared to that seen in benign lesions. Mann et al evaluated 160 patients and found that the maximum slope of malignancy in early enhancement outperformed the Breast Imaging and Reporting Data System (BI-RADS) (51) evaluation of the shape and internal contrast (AUC 0.829 vs. 0.692) (49). Abe et al evaluated the initial enhancement rate (IER) and signal enhancement ratio (SER) after aortic enhancement for malignant and benign lesions, with increased IER and SER noted in malignancy (47). Additional studies utilizing various ultrafast techniques have shown high reproducibility of early wash-in temporal kinetic parameters (33, 52, 53).

Importantly, these ultrafast techniques are easily incorporated into abbreviated breast MRI protocols (Figure 4), with ultrafast imaging acquired immediately postinjection to evaluate wash-in kinetics and a traditional high spatial resolution sequence subsequently acquired to allow for further evaluation of lesion shape and internal enhancement (47).

58-year-old woman with history of left lumpectomy and radiotherapy five years prior. MRI was performed for high-risk screening. Ultrafast TWIST images with 4 second temporal resolution after contrast injection performed on a 3.0T magnet demonstrates enhancement of the aorta at 4 seconds (A) and early wash-in of contrast in the left breast retroareolar region (arrow) at two frames (8 seconds) (B), which is highly suspicious for malignancy (49). First postcontrast subtraction images confirm abnormal retroareolar enhancement (C) and two abnormal axillary nodes (arrowhead) are seen on the maximum intensity projection (MIP) image (D). Punch skin biopsy of the breast and ultrasound-guided fine-needle aspiration of the axilla confirmed recurrent invasive ductal carcinoma with axillary nodal metastases.
Figure 4.

58-year-old woman with history of left lumpectomy and radiotherapy five years prior. MRI was performed for high-risk screening. Ultrafast TWIST images with 4 second temporal resolution after contrast injection performed on a 3.0T magnet demonstrates enhancement of the aorta at 4 seconds (A) and early wash-in of contrast in the left breast retroareolar region (arrow) at two frames (8 seconds) (B), which is highly suspicious for malignancy (49). First postcontrast subtraction images confirm abnormal retroareolar enhancement (C) and two abnormal axillary nodes (arrowhead) are seen on the maximum intensity projection (MIP) image (D). Punch skin biopsy of the breast and ultrasound-guided fine-needle aspiration of the axilla confirmed recurrent invasive ductal carcinoma with axillary nodal metastases.

ECOG-ACRIN trial results

The ECOG-ACRIN trial EA1141 comparison of abbreviated breast MRI and DBT in breast cancer screening in women with dense breasts (54) enrolled 1450 asymptomatic, average-risk women with dense breasts to undergo both DBT and abbreviated MRI screening exams on the same day; exclusion criteria included prior breast MRI. Follow-up is ongoing for another two years. Initial results from this multicenter prospective trial demonstrated that AB-MRI detected 17 of 17 invasive cancers and 5 of 6 DCIS for an invasive cancer detection rate (CDR) of 11.8 of 1000 women and an overall CDR of 15.2 of 1000 women. This was significantly higher than DBT, which had an invasive CDR of 4.8 of 1000 women and an overall CDR of 6.2 of 1000 women. No invasive cancers were detected by DBT alone. AB-MRI had more short-term follow-up recommendations (BI-RADS 3: probably benign) compared to DBT (7.5% vs. 1.2%). However, 10.1% of DBT exams required additional imaging (BI-RADS 0: needs additional imaging) compared to 0% of AB-MRI studies. Overall, the combined recommendation for additional imaging (BI-RADS 0 and 3) was not significantly different between AB-MRI and DBT (P = 0.02). Biopsy PPV was not significantly different between AB-MRI and DBT (P = 0.15). The EA1141 investigators will also evaluate the types of detected invasive and in situ cancers by genomic profiling to determine whether abbreviated MRI may identify more biologically aggressive tumors than DBT. Additional cost-effectiveness analysis is ongoing (17).

Abbreviated breast MRI in newly diagnosed breast cancer

Retrospective studies of cohorts of known breast cancer have demonstrated high sensitivity for detection of the primary malignancy. However, there is limited data on the ability of abbreviated MRI in the setting of evaluating the extent of disease. There is concern that the absence of the delayed postcontrast imaging in this setting may limit the evaluation of slowly enhancing lesions, such as DCIS or invasive lobular carcinoma (ILC). Lee-Felker et al evaluated an abbreviated protocol in 81 patients with known breast cancer (95 cancers, 11% ILC, average size 27 mm) and found no difference in contralateral malignancy, ipsilateral malignancy, or axillary nodal detection compared to a full protocol (P = 0.561 for cancer detection, 0.177 for nodal detection) (55). Individual readers had 3 to 6 false negative cases per reader without prior imaging and 0 to 3 with prior imaging. Missed cancers were DCIS or low-grade IDC, similar to that observed in prior studies of known cancer (19, 22).

Limitations of abbreviated breast MRI

Although abbreviated MRI demonstrates sensitivity and specificity for breast cancer detection similar to that of a full breast MRI protocol, there are limitations. Axillary lesions may be missed on MIP images (Figure 5); careful review of the subtraction images is recommended to avoid this pitfall (19, 22). The absence of delayed postcontrast imaging limits the evaluation of slow-enhancing malignancies (Figure 6). Although ultrafast imaging appears to assist in the detection of pure DCIS (33), retrospective analysis of missed known cancers on abbreviated MRI suggests that DCIS is less likely to be detected on abbreviated MRI compared to delayed postcontrast sequences (19, 22). Delayed postcontrast imaging also has an important role in postneoadjuvant chemotherapy follow-up, with increased accuracy for evaluating residual tumor size compared to early postcontrast sequences (10, 56).

61-year-old woman with new diagnosis of left axillary tail invasive ductal carcinoma. There is an irregular, heterogeneously enhancing mass in the left axillary tail (arrow) with associated pectoralis fascia enhancement less well seen on the maximum intensity projection (MIP) image (A) than on first postcontrast T1-weighted images (B) and corresponding subtraction images (C), with increased T2 signal intensity (D). This axillary lesion is not well seen on the MIP images, a known limitation of abbreviated MRI and MIP image interpretation (19).
Figure 5.

61-year-old woman with new diagnosis of left axillary tail invasive ductal carcinoma. There is an irregular, heterogeneously enhancing mass in the left axillary tail (arrow) with associated pectoralis fascia enhancement less well seen on the maximum intensity projection (MIP) image (A) than on first postcontrast T1-weighted images (B) and corresponding subtraction images (C), with increased T2 signal intensity (D). This axillary lesion is not well seen on the MIP images, a known limitation of abbreviated MRI and MIP image interpretation (19).

45-year-old woman with new diagnosis of invasive lobular cancer in the right breast at 11 o’clock. MRI was performed to evaluate the extent of disease. Maximum intensity projection (MIP) image (A) demonstrates marked background parenchymal enhancement with no abnormal enhancement. There is subtle focal nonmass enhancement in the right breast at 11 o’clock middle depth (arrow), superior and lateral to the biopsy clip artifact (arrowhead) on first postcontrast subtraction images (B) without definite increased T2-weighted signal (C). Abbreviated breast MRI may be limited in the setting of marked background parenchymal enhancement and in the evalution of lobular carcinomas (19, 22), which often demonstrate delayed or subtle contrast wash-in due to their lower angiogenesis and single-file cellular growth pattern compared with invasive ductal carcinoma. The enhancement of the cancer is slightly better appreciated on delayed postcontrast images (D) but is still partially masked by background parenchymal enhancement.
Figure 6.

45-year-old woman with new diagnosis of invasive lobular cancer in the right breast at 11 o’clock. MRI was performed to evaluate the extent of disease. Maximum intensity projection (MIP) image (A) demonstrates marked background parenchymal enhancement with no abnormal enhancement. There is subtle focal nonmass enhancement in the right breast at 11 o’clock middle depth (arrow), superior and lateral to the biopsy clip artifact (arrowhead) on first postcontrast subtraction images (B) without definite increased T2-weighted signal (C). Abbreviated breast MRI may be limited in the setting of marked background parenchymal enhancement and in the evalution of lobular carcinomas (19, 22), which often demonstrate delayed or subtle contrast wash-in due to their lower angiogenesis and single-file cellular growth pattern compared with invasive ductal carcinoma. The enhancement of the cancer is slightly better appreciated on delayed postcontrast images (D) but is still partially masked by background parenchymal enhancement.

Abbreviated MRI as a value initiative

The abbreviated MRI exam has been embraced in the radiology community as an important valuable initiative. It has been evaluated to screen for prostate cancer and hepatocellular carcinoma, to reduce scan time and sedation in pediatric body MRI, and to evaluate for stress fractures and osteomyelitis (57–59). Although heterogeneous imaging protocols were utilized, these studies show comparable diagnostic accuracies to the full protocol (57–59).

The blitz of abbreviated MRI studies reflects the increasing scrutiny of the disproportionate contribution of radiology to the rising overall healthcare expenditures (60). Healthcare policy makers are focused on curbing the use of advanced imaging examinations, such as MRI, while continuing to promote the quality and appropriateness of imaging. Value-based healthcare has quickly replaced the fee-for-service model. These policy changes have led to a variety of new metrics that are being imposed on radiology providers (61, 62). An important cornerstone of value-based healthcare defines value as the patient’s outcome over costs (63). It is anticipated that abbreviated MRI exams may be cost-effective compared to other breast imaging screening modalities (17), which is important with the recent development of metrics that measure the radiologist’s impact on patient outcomes. These metrics will measure a radiologist’s contribution to reducing costs and improving patient outcomes with the intention of making reimbursement commensurate with adherence to these metrics (64). Therefore, the concept of a fast, abbreviated MRI exam is appealing given its high diagnostic accuracy coupled with the possibility of a marked reduction in the cost of an MRI examination (60).

Reimbursement for an abbreviated breast MRI examination

An unresolved issue is the reimbursement for abbreviated MRI exams because these initial results need to be validated by other studies. There is no CPT code for an abbreviated MRI examination. Some imaging facilities (eg, University of Pennsylvania, Case Western University) that perform a clinical abbreviated breast MRI examination inform patients that the study is self-pay and will not be billed to insurance (65). Other issues that will affect reimbursement include the expected scan time and whether a gadolinium contrast agent is necessary. A secondary aim of the ECOG-ACRIN 1141 trial is to perform a comparative cost analysis comparing an abbreviated exam to DBT (54). Although the hypothetical cost of an abbreviated breast MRI is still being explored, a reasonable fee should be comparable with other breast imaging screening exams. For instance, Plecha and colleagues thoughtfully used other radiology self-pay screening tests at their institution, such as unenhanced lung cancer CT screening and cardiac scoring, as precedents to determine the pricing of their abbreviated breast MRI exam (66). The final cost is substantially lower than that of the full breast MRI protocol and many patients with high-deductible insurance plans have a lower out-of-pocket expense for abbreviated breast MRI than for the full protocol. Throughout their system, the authors have Fast MRI (the name they gave the examination) hours embedded in MRI schedules.

Challenges with clinical implementation of an abbreviated MRI examination

Another unresolved issue is how an abbreviated breast MRI exam will be implemented in the clinical workflow. From an operations viewpoint, it is clear that “scan time” is not equivalent to “table time.” This information is critical to estimating the price point for an abbreviated MR exam.

In their recent paper “Comparison of Study Activity Times for ‘Full’ versus ‘Fast MRI’ for Breast Cancer Screening,” Borthakur et al analyzed the activity times from 70 abbreviated breast MRI studies and 736 full MR screening studies (67). The total scan time was divided into actual scan time and nonscan-related technologist activity time. The authors found the actual scan time for the AB protocol was 17.5 minutes compared with 28.8 minutes for the full protocol, (difference, 11.3 min; P < 0.0001). The total study time was 36 minutes for AB-MRI and 50 minutes for the full protocol (difference, 13.7 min; P < 0.0001), implying that the AB-MR protocol had only a 38% greater patient flow rate than the full protocol. These results are not entirely unexpected because the calculated scan times do not reflect other workflow considerations such as setup and positioning of the patient, room turnover, safety screening, and IV placement that must be considered. Borthakur and colleagues concluded that the realized gains in patient flow rate (38% for abbreviated MRI compared to a full protocol) were lower than expected based on scan time decrease (65%) because of the increased technologist activity time for the AB-MR protocol (67).

The above results suggest that optimization of MRI workflow may be key to adding value. Practical solutions may include keeping the breast coil on the table when imaging several patients consecutively. For example, Plecha and colleagues schedule three 10-minute AB-MR examinations in a 1-hour time slot, the time allotted for one full-protocol MRI examination (66). However, as hardware and software advances in MRI have significantly decreased acquisition and room times, turnaround time now is of increasing importance. At our institution, significant inefficiencies were removed with the utilization of dockable tables, dedicated MRI patient preparation rooms, two doors in each MRI room, positioning the scanner to provide the most direct path to the scanner, and coil storage in the preparation rooms, with duplication of the most frequently used coils (68). The optimized workflow resulted in a mean time savings of 5 minutes and 28 seconds per patient. Shorter turnaround times would allow an increased number of available examination time slots per MRI scanner. This would increase the value of MRI by increasing the availability of MRI for patients, increasing the productivity of each scanner and the technical teams, decreasing the time patients need to be in the MRI department, and providing increased revenue (68).

Finally, another aspect of an abbreviated MRI exam that needs to be considered is that, although in the study setting reading times can be substantially shortened, it has to be seen where this will translate into clinical reality where an MRI interpretation includes reviewing the patient’s history and prior examinations. In summary, although further larger-scale studies and rigorous standardization is necessary, initial results support the feasibility of offering a cost-effective screening breast DCE-MRI to a broader population.

Future directions

Although the results from previous studies investigating abbreviated MRI protocols are promising, they might not be generalizable to a broad population. To date, these protocols have been investigated mainly for breast cancer screening. The utility of abbreviated breast MRI has yet to be fully evaluated in preoperative MRI staging to assess for the extent of local disease, assessing response to neoadjuvant chemotherapy response, or for problem solving.

Research is ongoing to evaluate specific applications of abbreviated breast MRI. Choi et al performed 799 AB-MRI examinations in 725 women with a history of breast cancer surgery (34). The image acquisition time was 8.5 minutes. AB-MRI detected 12 malignancies in 12 women (15.0 cancers per 1000 cases). Seven of these 12 malignancies were initially undetected on ultrasound and mammography, although subsequent MRI-detected ultrasound revealed lesions corresponding to the MRI-detected lesions. The PPVs for recall and biopsy and sensitivity and specificity values for screening MRI were 12.4%, 61.5%, 100%, and 89.2%, respectively. This has led to an ongoing prospective multicenter trial using abbreviated MRI (clinicaltrials.gov Identifier: NCT03475979) in Korea. Breast cancer gene (BRCA) mutation carriers with a history of breast cancer surgery will be screened with 2 rounds of mammography, ultrasound, and abbreviated MRI, with a target enrollment of 1600 women (69). The primary endpoint is to compare the cancer detection rates and false positive rates in BRCA mutation carriers with noncarriers for each screening modality. Researchers will also compare mammography, ultrasound, and abbreviated MRI in patients with BRCA mutations and in those treated for breast cancer. In addition, they will analyze the characteristics of subsequent cancer over a five-year follow-up period (69). A similar prospective study evaluates abbreviated breast MRI in women who are status postprimary breast cancer treated with breast conservation therapy three years prior to recruitment. The study is being performed at the University of Pennsylvania (NCT03664778), with a targeted accrual of 500 patients.

Other novel research protocols include comparing the role of abbreviated breast MRI to DWI of the breast for breast cancer screening and comparing abbreviated MRI to contrast-enhanced spectral mammography for breast cancer screening. There may also be a role for synthetic MRI reconstruction and the use of deep-learning tools for MR reconstruction to provide more information. An ongoing study at our institution, NCT03927768, explores the feasibility of a golden-angle radial compressed sensing and parallel imaging to assess the wash-in of contrast utilizing ultrafast imaging. Finally, the PRISM: PRImary Screening with MRI Prospective randomly assigned trial is being developed by ECOG-ACRIN, which compares DBT and whole breast screening MRI to abbreviated MRI.

Conclusion

Abbreviated breast MRI offers decreased scan time and cost, increased patient tolerance, and increased accessibility of breast MRI screening to patients with an intermediate and high lifetime risk of breast cancer. Studies to date have shown high reproducibility of its high sensitivity in varied screening populations across the world, but most are retrospective. Future results from multicenter clinical trials are likely to confirm that abbreviated MRI offers improved cancer detection than DBT in patients at increased risk and with dense breasts. Although further large-scale studies and protocol standardization are still needed, the increased cancer detection that abbreviated breast MRI offers is an important step forward in breast cancer screening.

Funding

Radiological Society of North America Seed Grant (L.H.).

Conflict of interest statement

None declared.

References

1.

Myers
ER
,
Moorman
P
,
Gierisch
JM
, et al.
Benefits and harms of breast cancer screening: a systematic review
.
JAMA
2015
;
314
(
15
):
1615
1634
.

2.

Monticciolo
DL
,
Newell
MS
,
Hendrick
RE
, et al.
Breast cancer screening for average-risk women: recommendations from the ACR Commission on Breast Imaging
.
J Am Coll Radiol
2017
;
14
(
9
):
1137
1143
.

3.

Sardanelli
F
,
Aase
HS
,
Álvarez
M
, et al.
Position paper on screening for breast cancer by the European Society of Breast Imaging (EUSOBI) and 30 national breast radiology bodies from Austria, Belgium, Bosnia and Herzegovina, Bulgaria, Croatia, Czech Republic, Denmark, Estonia, Finland, France, Germany, Greece, Hungary, Iceland, Ireland, Italy, Israel, Lithuania, Moldova, The Netherlands, Norway, Poland, Portugal, Romania, Serbia, Slovakia, Spain, Sweden, Switzerland and Turkey
.
Eur Radiol
2017
;
27
(
7
):
2737
2743
.

4.

Pisano
ED
,
Gatsonis
C
,
Hendrick
E
, et al.
Digital Mammographic Imaging Screening Trial (DMIST) Investigators Group
.
Diagnostic performance of digital versus film mammography for breast-cancer screening
.
N Engl J Med
2005
;
353
(
17
):
1773
1783
.

5.

McCarthy
AM
,
Barlow
WE
,
Conant
EF
, et al. ;
PROSPR Consortium
.
Breast cancer with a poor prognosis diagnosed after screening mammography with negative results
.
JAMA Oncol
2018
;
4
(
7
):
998
1001
.

6.

Sung
JS
,
Stamler
S
,
Brooks
J
, et al.
Breast cancers detected at screening MR imaging and mammography in patients at high risk: method of detection reflects tumor histopathologic results
.
Radiology
2016
;
280
(
3
):
716
722
.

7.

Lehman
CD
,
Isaacs
C
,
Schnall
MD
, et al.
Cancer yield of mammography, MR, and US in high-risk women: prospective multi-institution breast cancer screening study
.
Radiology
2007
;
244
(
2
):
381
388
.

8.

Berg
WA
,
Zhang
Z
,
Lehrer
D
, et al. ;
ACRIN 6666 Investigators
.
Detection of breast cancer with addition of annual screening ultrasound or a single screening MRI to mammography in women with elevated breast cancer risk
.
JAMA
2012
;
307
(
13
):
1394
1404
.

9.

Kuhl
C
,
Weigel
S
,
Schrading
S
, et al.
Prospective multicenter cohort study to refine management recommendations for women at elevated familial risk of breast cancer: the EVA trial
.
J Clin Oncol
2010
;
28
(
9
):
1450
1457
.

10.

Mann
RM
,
Cho
N
,
Moy
L
.
Breast MRI: state of the art
.
Radiology
2019
;
292
(
3
):
520
536
.

11.

Monticciolo
DL
,
Newell
MS
,
Moy
L
,
Niell
B
,
Monsees
B
,
Sickles
EA
.
Breast cancer screening in women at higher-than-average risk: recommendations from the ACR
.
J Am Coll Radiol
2018
;
15
(
3 Pt A
):
408
414
.

12.

Berg
WA
,
Blume
JD
,
Adams
AM
, et al.
Reasons women at elevated risk of breast cancer refuse breast MR imaging screening: ACRIN 6666
.
Radiology
2010
;
254
(
1
):
79
87
.

13.

Wernli
KJ
,
DeMartini
WB
,
Ichikawa
L
, et al. ;
Breast Cancer Surveillance Consortium
.
Patterns of breast magnetic resonance imaging use in community practice
.
JAMA Intern Med
2014
;
174
(
1
):
125
132
.

14.

Kuhl
CK
,
Schrading
S
,
Strobel
K
,
Schild
HH
,
Hilgers
RD
,
Bieling
HB
.
Abbreviated breast magnetic resonance imaging (MRI): first postcontrast subtracted images and maximum-intensity projection-a novel approach to breast cancer screening with MRI
.
J Clin Oncol
2014
;
32
(
22
):
2304
2310
.

15.

Cohen
RA
,
Zammitti
EP.
High-Deductible Health Plan Enrollment among Adults Aged 18–64 with Employment-based Insurance Coverage
., in NCHS Data Brief,
no 317
.
Hyattsville, MD
:
National Center for Health Statistics
,
2018
. https://www.cdc.gov/nchs/products/databriefs/db317.htm. Accessed 9 April 2020.

16.

Onega
T
,
Lee
CI
,
Benkeser
D
, et al.
Travel burden to breast MRI and utilization: are risk and sociodemographics related?
J Am Coll Radiol
2016
;
13
(
6
):
611
619
.

17.

Comstock
CE
,
Gatsonis
C
,
Newstead
GM
, et al.
Comparison of abbreviated breast MRI vs digital breast tomosynthesis for breast cancer detection among women with dense breasts undergoing screening
.
JAMA
2020
;
323
(
8
):
746
756
.

18.

ACR
.
American College of Radiology website. Breast magnetic resonance imaging (MRI) accreditation program requirements
.
2017
; Available at: www.acraccreditation.org/~/media/ACRAccreditation/Documents/Breast-MRI/Requirements.pdf?la=en. Accessed 17 October 2019.

19.

Mango
VL
,
Morris
EA
,
David Dershaw
D
, et al.
Abbreviated protocol for breast MRI: are multiple sequences needed for cancer detection?
Eur J Radiol
2015
;
84
(
1
):
65
70
.

20.

Grimm
LJ
,
Soo
MS
,
Yoon
S
,
Kim
C
,
Ghate
SV
,
Johnson
KS
.
Abbreviated screening protocol for breast MRI: a feasibility study
.
Acad Radiol
2015
;
22
(
9
):
1157
1162
.

21.

Partridge
SC
,
Stone
KM
,
Strigel
RM
,
DeMartini
WB
,
Peacock
S
,
Lehman
CD
.
Breast DCE-MRI: influence of postcontrast timing on automated lesion kinetics assessments and discrimination of benign and malignant lesions
.
Acad Radiol
2014
;
21
(
9
):
1195
1203
.

22.

Heacock
L
,
Melsaether
AN
,
Heller
SL
, et al.
Evaluation of a known breast cancer using an abbreviated breast MRI protocol: correlation of imaging characteristics and pathology with lesion detection and conspicuity
.
Eur J Radiol
2016
;
85
(
4
):
815
823
.

23.

Moschetta
M
,
Telegrafo
M
,
Rella
L
,
Stabile Ianora
AA
,
Angelelli
G
.
Abbreviated combined mr protocol: a new faster strategy for characterizing breast lesions
.
Clin Breast Cancer
2016
;
16
(
3
):
207
211
.

24.

Machida
Y
,
Shimauchi
A
,
Kanemaki
Y
,
Igarashi
T
,
Harada
M
,
Fukuma
E
.
Feasibility and potential limitations of abbreviated breast MRI: an observer study using an enriched cohort
.
Breast Cancer
2017
;
24
(
3
):
411
419
.

25.

Oldrini
G
,
Derraz
I
,
Salleron
J
,
Marchal
F
,
Henrot
P
.
Impact of an abbreviated protocol for breast MRI in diagnostic accuracy
.
Diagn Interv Radiol
2018
;
24
(
1
):
12
16
.

26.

Panigrahi
B
,
Mullen
L
,
Falomo
E
,
Panigrahi
B
,
Harvey
S
.
An abbreviated protocol for high-risk screening breast magnetic resonance imaging: impact on performance metrics and BI-RADS assessment
.
Acad Radiol
2017
;
24
(
9
):
1132
1138
.

27.

Romeo
V
,
Cuocolo
R
,
Liuzzi
R
, et al.
Preliminary results of a simplified breast MRI protocol to characterize breast lesions: comparison with a full diagnostic protocol and a review of the current literature
.
Acad Radiol
2017
;
24
(
11
):
1387
1394
.

28.

Harvey
SC
,
Di Carlo
PA
,
Lee
B
,
Obadina
E
,
Sippo
D
,
Mullen
L
.
An abbreviated protocol for high-risk screening breast MRI saves time and resources
.
J Am Coll Radiol
2016
;
13
(
4
):
374
380
.

29.

Ballesio
L
,
Savelli
S
,
Angeletti
M
, et al.
Breast MRI: are T2 IR sequences useful in the evaluation of breast lesions?
Eur J Radiol
2009
;
71
(
1
):
96
101
.

30.

Kuhl
CK
,
Klaschik
S
,
Mielcarek
P
,
Gieseke
J
,
Wardelmann
E
,
Schild
HH
.
Do T2-weighted pulse sequences help with the differential diagnosis of enhancing lesions in dynamic breast MRI?
J Magn Reson Imaging
1999
;
9
(
2
):
187
196
.

31.

Kelcz
F
.
Quantitative assessment of T2 imaging information in differential diagnosis of enhancing breast lesions
.
Eur Radiol
2006
;
16
(
Suppl 5
):
E51
E53
.

32.

Mann
RM
,
Kuhl
CK
,
Kinkel
K
,
Boetes
C
.
Breast MRI: guidelines from the European Society of Breast Imaging
.
Eur Radiol
2008
;
18
(
7
):
1307
1318
.

33.

Oldrini
G
,
Fedida
B
,
Poujol
J
, et al.
Abbreviated breast magnetic resonance protocol: value of high-resolution temporal dynamic sequence to improve lesion characterization
.
Eur J Radiol
2017
;
95
:
177
185
.

34.

Choi
BH
,
Choi
N
,
Kim
MY
,
Yang
JH
,
Yoo
YB
,
Jung
HK
.
Usefulness of abbreviated breast MRI screening for women with a history of breast cancer surgery
.
Breast Cancer Res Treat
2018
;
167
(
2
):
495
502
.

35.

Dogan
BE
,
Scoggins
ME
,
Son
JB
, et al.
American College of Radiology-compliant short protocol breast MRI for high-risk breast cancer screening: a prospective feasibility study
.
AJR Am J Roentgenol
2018
;
210
(
1
):
214
221
.

36.

Strahle
DA
,
Pathak
DR
,
Sierra
A
,
Saha
S
,
Strahle
C
,
Devisetty
K
.
Systematic development of an abbreviated protocol for screening breast magnetic resonance imaging
.
Breast Cancer Res Treat
2017
;
162
(
2
):
283
295
.

37.

Petrillo
A
,
Fusco
R
,
Sansone
M
, et al.
Abbreviated breast dynamic contrast-enhanced MR imaging for lesion detection and characterization: the experience of an Italian oncologic center
.
Breast Cancer Res Treat
2017
;
164
(
2
):
401
410
.

38.

Runge
VM
.
Safety of the gadolinium-based contrast agents for magnetic resonance imaging, focusing in part on their accumulation in the brain and especially the dentate nucleus
.
Invest Radiol
2016
;
51
(
5
):
273
279
.

39.

Gulani
V
,
Calamante
F
,
Shellock
FG
,
Kanal
E
,
Reeder
SB
;
International Society for Magnetic Resonance in Medicine
.
Gadolinium deposition in the brain: summary of evidence and recommendations
.
Lancet Neurol
2017
;
16
(
7
):
564
570
.

40.

Bennani-Baiti
B
, et al.
Evaluation of 3.0-T MRI brain signal after exposure to gadoterate meglumine in women with high breast cancer risk and screening breast MRI
.
Radiology
2019
;293(3):523–530
.

41.

Yabuuchi
H
,
Matsuo
Y
,
Sunami
S
, et al.
Detection of non-palpable breast cancer in asymptomatic women by using unenhanced diffusion-weighted and T2-weighted MR imaging: comparison with mammography and dynamic contrast-enhanced MR imaging
.
Eur Radiol
2011
;
21
(
1
):
11
17
.

42.

McDonald
ES
,
Hammersley
JA
,
Chou
SH
, et al.
Performance of DWI as a rapid unenhanced technique for detecting mammographically occult breast cancer in elevated-risk women with dense breasts
.
AJR Am J Roentgenol
2016
;
207
(
1
):
205
216
.

43.

Trimboli
RM
,
Verardi
N
,
Cartia
F
,
Carbonaro
LA
,
Sardanelli
F
.
Breast cancer detection using double reading of unenhanced MRI including T1-weighted, T2-weighted STIR, and diffusion-weighted imaging: a proof of concept study
.
AJR Am J Roentgenol
2014
;
203
(
3
):
674
681
.

44.

Bickelhaupt
S
,
Laun
FB
,
Tesdorff
J
, et al.
Fast and noninvasive characterization of suspicious lesions detected at breast cancer X-ray screening: capability of diffusion-weighted MR imaging with MIPs
.
Radiology
2016
;
278
(
3
):
689
697
.

45.

Pinker
K
,
Moy
L
,
Sutton
EJ
, et al.
Diffusion-weighted imaging with apparent diffusion coefficient mapping for breast cancer detection as a stand-alone parameter: comparison with dynamic contrast-enhanced and multiparametric magnetic resonance imaging
.
Invest Radiol
2018
;
53
(
10
):
587
595
.

46.

Chen
SQ
,
Huang
M
,
Shen
YY
,
Liu
CL
,
Xu
CX
.
Abbreviated MRI protocols for detecting breast cancer in women with dense breasts
.
Korean J Radiol
2017
;
18
(
3
):
470
475
.

47.

Abe
H
,
Mori
N
,
Tsuchiya
K
, et al.
Kinetic analysis of benign and malignant breast lesions with ultrafast dynamic contrast-enhanced MRI: comparison with standard kinetic assessment
.
AJR Am J Roentgenol
2016
;
207
(
5
):
1159
1166
.

48.

Heacock
L
,
Gao
Y
,
Heller
SL
, et al.
Comparison of conventional DCE-MRI and a novel golden-angle radial multicoil compressed sensing method for the evaluation of breast lesion conspicuity
.
J Magn Reson Imaging
2017
;
45
(
6
):
1746
1752
.

49.

Mann
RM
,
Mus
RD
,
van Zelst
J
,
Geppert
C
,
Karssemeijer
N
,
Platel
B
.
A novel approach to contrast-enhanced breast magnetic resonance imaging for screening: high-resolution ultrafast dynamic imaging
.
Invest Radiol
2014
;
49
(
9
):
579
585
.

50.

Jimenez
JE
,
Strigel
RM
,
Johnson
KM
,
Henze Bancroft
LC
,
Reeder
SB
,
Block
WF
.
Feasibility of high spatiotemporal resolution for an abbreviated 3D radial breast MRI protocol
.
Magn Reson Med
2018
;
80
(
4
):
1452
1466
.

51.

Morris
EA
, Comstock C,
Lee
CH
.
ACR BI-RADS® magnetic resonance imaging.
In:
ACR BI-RADS® Atlas, Breast Imaging Reporting and Data System
.
Reston, VA
:
American College of Radiology
,
2013
.

52.

Pineda
FD
,
Medved
M
,
Wang
S
, et al.
Ultrafast bilateral DCE-MRI of the breast with conventional fourier sampling: preliminary evaluation of semi-quantitative analysis
.
Acad Radiol
2016
;
23
(
9
):
1137
1144
.

53.

Platel
B
,
Mus
R
,
Welte
T
,
Karssemeijer
N
,
Mann
R
.
Automated characterization of breast lesions imaged with an ultrafast DCE-MR protocol
.
IEEE Trans Med Imaging
2014
;
33
(
2
):
225
232
.

54.

Kuhl
CK
.
Abbreviated breast MRI for screening women with dense breast: the EA1141 trial
.
Br J Radiol
2018
;
91
(
1090
):
20170441
.

55.

Lee-Felker
S
,
Joines
M
,
Storer
L
, et al.
Abbreviated breast MRI for estimating extent of disease in newly diagnosed breast cancer
.
J Breat Imag
2019
;
2
(
1
):
43
49
.

56.

Kim
SY
,
Cho
N
,
Park
IA
, et al.
Dynamic contrast-enhanced breast mRI for evaluating residual tumor size after neoadjuvant chemotherapy
.
Radiology
2018
;
289
(
2
):
327
334
.

57.

Canellas
R
,
Rosenkrantz
AB
,
Taouli
B
, et al.
Abbreviated MRI Protocols for the Abdomen
.
Radiographics
2019
;
39
(
3
):
744
758
.

58.

Ahmad
R
,
Hu
HH
,
Krishnamurthy
R
,
Krishnamurthy
R
.
Reducing sedation for pediatric body MRI using accelerated and abbreviated imaging protocols
.
Pediatr Radiol
2018
;
48
(
1
):
37
49
.

59.

Khurana
B
,
Okanobo
H
,
Ossiani
M
,
Ledbetter
S
,
Al Dulaimy
K
,
Sodickson
A
.
Abbreviated MRI for patients presenting to the emergency department with hip pain
.
AJR Am J Roentgenol
2012
;
198
(
6
):
W581
W588
.

60.

Leithner
D
,
Moy
L
,
Morris
EA
,
Marino
MA
,
Helbich
TH
,
Pinker
K
.
Abbreviated MRI of the breast: does it provide value?
J Magn Reson Imaging
2019
;
49
(
7
):
e85
e100
.

61.

Rubin
GD
.
Costing in radiology and health care: rationale, relativity, rudiments, and realities
.
Radiology
2017
;
282
(
2
):
333
347
.

62.

McGinty
G
.
Is value-driven health care an unfunded mandate for radiologists?
AJR Am J Roentgenol
2016
;
206
(
2
):
280
282
.

63.

European Society of R.
ESR concept paper on value-based radiology
.
Insights Imaging
2017
;
8
(
5
):
447
454
.

64.

Sarwar
A
,
Boland
G
,
Monks
A
,
Kruskal
JB
.
Metrics for radiologists in the era of value-based health care delivery
.
Radiographics
2015
;
35
(
3
):
866
876
.

65.

Medicine, P
.
FAQs about mammograms, including 2D and 3D mammograms, ABUS and fast breast MRI
.
2018
. 11/4/2019; Available at: https://www.pennmedicine.org/cancer/about/focus-on-cancer/2018/october/faq-about-breast-cancer-screening-at-penn. Accessed 11 April 2020.

66.

Marshall
H
, et al.
Implementing abbreviated MRI screening into a breast imaging practice
.
AJR Am J Roentgenol
2019
;213(1):234–237 .

67.

Borthakur
A
,
Weinstein
SP
,
Schnall
MD
,
Conant
EF
.
Comparison of study activity times for “full” versus “fast MRI” for breast cancer screening
.
J Am Coll Radiol
2019
;
16
(
8
):
1046
1051
.

68.

Recht
MP
,
Block
KT
,
Chandarana
H
, et al.
Optimization of MRI turnaround times through the use of dockable tables and innovative architectural design strategies
.
AJR Am J Roentgenol
2019
;
212
(
4
):
855
858
.

69.

Ko
ES
,
Morris
EA
.
Abbreviated magnetic resonance imaging for breast cancer screening: concept, early results, and considerations
.
Korean J Radiol
2019
;
20
(
4
):
533
541
.

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