Quantitative Diffusion-Weighted Imaging as an Adjunct to Conventional Breast MRI for Improved Positive Predictive Value
Abstract
OBJECTIVE. The purpose of our study was to investigate whether adding diffusion-weighted imaging (DWI) to dynamic contrast-enhanced MRI (DCE-MRI) could improve the positive predictive value (PPV) of breast MRI.
MATERIALS AND METHODS. The retrospective study included 70 women with 83 suspicious breast lesions on DCE-MRI (BI-RADS 4 or 5) who underwent subsequent biopsy. DWI was acquired during clinical breast MRI using b = 0 and 600 s/mm2. Apparent diffusion coefficient (ADC) values were compared for benign and malignant lesions. PPV was calculated for DCE-MRI alone (based on biopsy recommendations) and DCE-MRI plus DWI (adding an ADC threshold) for the same set of lesions. Results were further compared by lesion type (mass, nonmasslike enhancement) and size.
RESULTS. Of the 83 suspicious lesions, 52 were benign and 31 were malignant (11 ductal carcinoma in situ [DCIS], 20 invasive carcinoma). Both DCIS (mean ADC, 1.31 ± 0.24 × 10–3 mm2/s) and invasive carcinoma (mean ADC, 1.29 ± 0.29 × 10–3 mm2/s) exhibited lower mean ADC than benign lesions (1.70 ± 0.44 × 10–3 mm2/s, p < 0.001). Applying an ADC threshold of 1.81 × 10–3 mm2/s for 100% sensitivity produced a PPV of 47% versus 37% for DCE-MRI alone, which would have avoided biopsy for 33% (17/52) of benign lesions without missing any cancers. DWI increased PPV similarly for masses and nonmasslike enhancement and preferentially improved PPV for smaller (≤ 1 cm) versus larger lesions.
CONCLUSION. DWI shows potential for improving the PPV of breast MRI for lesions of varied types and sizes. However, considerable overlap in ADC of benign and malignant lesions necessitates validation of these findings in larger studies.
Introduction
Dynamic contrast-enhanced MRI (DCE-MRI) of the breast has a high sensitivity for breast cancer detection and has recently been shown to be the most sensitive breast screening technique for women at high risk [1–4]. DCE-MRI is also more accurate than mammography or ultrasound for the delineation of the extent of disease in patients with a recent diagnosis of cancer [5–8]. The high sensitivity of clinical breast DCE-MRI results primarily from the differential enhancement between normal and malignant tissue on T1-weighted imaging. However, the moderate specificity of DCE-MRI using current morphologic and kinetic enhancement criteria can present additional challenges also by detecting many benign lesions.
A review of six studies to screen women at high risk for breast cancer found a wide variation in the positive predictive value (PPV) of breast MRI [9]. Calculated as the percentage of lesions deemed suspicious on MRI and found to be malignant on biopsy, PPV ranged from 24% to 89%. Studies investigating MRI for breast cancer staging report similar variability in PPV, with a recent meta-analysis of 19 studies showing PPV to range from 19% to 100% for detection of multifocal and multicentric disease [10]. A large scale study showing the value of MRI for detecting contralateral disease in patients with recently diagnosed breast cancer reported a PPV for MRI of 25% [7], with 91 false-positive findings among 121 biopsies performed as a result of suspicious findings on MRI. Techniques to improve the specificity of breast MRI could reduce unnecessary biopsies and thus improve the overall accuracy of this highly sensitive tool for detecting breast cancer.
Diffusion-weighted imaging (DWI) is an unenhanced MRI sequence that measures the mobility of water molecules in vivo and provides different and potentially complementary information to DCE-MRI. DWI is sensitive to biophysical characteristics of tissues, such as cell density, membrane integrity, and micro-structure [11]. Promising findings from preliminary DWI studies of the breast have shown significantly lower apparent diffusion coefficient (ADC) measures for breast carcinomas than for benign breast lesions or normal tissue [12–19]. The lower ADC in malignancies is primarily attributed to higher cell density causing increased restriction of the extracellular matrix and increased fraction of signal coming from intracellular water [12, 13, 20, 21]. A recent study reported high accuracy for characterizing enhancing breast masses through a multivariate combination of DWI and DCE-MRI features [22]. However this study did not include lesions described as nonmasslike enhancement, and the improvement in diagnostic accuracy over DCE-MRI alone was not assessed.
To our knowledge, no published studies have assessed the added diagnostic value of ADC measures to conventional breast MRI assessment in the discrimination of suspicious MRI-detected lesions. The purpose of this study was to investigate whether the addition of DWI to DCE-MRI could improve the PPV for suspicious lesions detected on breast MRI.
Materials and Methods
The protocol for this study was approved by our institutional review board and was compliant with HIPAA. A retrospective review of our prospectively populated MRI database was performed to identify all consecutive suspicious breast lesions detected on breast MRI from October 2005 to November 2006 (during which time DWI was acquired in clinical breast MRI examinations) that underwent subsequent core needle or surgical biopsy. Patients were required to be at least 18 years old and not undergoing neoadjuvant treatment.
Subjects and Lesions
Study lesions were those that were detected on breast MRI and assigned a final BI-RADS [23]) assessment of 4 (suspicious) or 5 (highly suggestive of malignancy), had DWI acquired successfully during MRI, and underwent core needle biopsy (ultrasound- or MRI-guided) or excision after MRI. Final histopathologic outcomes for lesions yielding high-risk atypical ductal hyperplasia (ADH) at core needle biopsy were based on subsequent surgical biopsy results. Lesions with BI-RADS assessments of 4 or 5 that did not go on to biopsy were excluded. BI-RADS 6 lesions (biopsy-proven, known malignancy at the time of MRI) were not included in this study.
One hundred twenty-three suspicious lesions (BI-RADS 4 or 5) with subsequent tissue sampling were identified on 103 DCE-MRI examinations in 102 women over the course of the study period. DWI was not performed in the MRI examinations for 25 of 123 (20%) lesions due to time constraints. Eleven of 98 lesions with DWI findings were excluded from the study because of technical problems with the DWI sequences resulting from patient motion (n = 10) or inadequate fat suppression (n = 1). Four lesions with ADH at core needle biopsy were excluded because they did not undergo subsequent surgical excision. Therefore, the final cohort included 83 lesions in 71 examinations in 70 women. Subjects ranged in age from 27 to 85 years (median, 52 years). The clinical indications for the examinations were to evaluate extent of disease in a patient with a new diagnosis of breast cancer in 36 of 71 (51%), high-risk screening in 28 of 71 (39%), problem solving in five of 71 (7%), and short-term follow-up in two of 71 (3%). The study lesions detected in newly diagnosed cancer or to evaluate extent of disease in patients constituted additional lesions distinct from the known, biopsy-proven cancers.
MRI Acquisition
All MRI was performed on an LX 1.5-T scanner with a dedicated 8-channel bilateral breast coil (GE Healthcare). Each MRI examination included a T2-weighted fast spin-echo sequence, T1-weighted non-fat-suppressed sequence, T1-weighted DCE-MRI sequence with one unenhanced and multiple contrast-enhanced scans, and a DWI sequence. All series were performed in the axial orientation to enable full bilateral coverage with the minimum scanning time.
DCE-MRI was acquired with a T1-weighted 3D fast spoiled gradient-recalled echo sequence with parallel imaging (VIBRANT, GE Healthcare) with the following parameters: TR/TE, 6.2/3; flip angle, 10°, and field of view, 32–38 cm. From October 2005 through June 2006, scanning was performed with 2.2-mm slice thickness, 350 × 350 matrix, and five contrast-enhanced acquisitions centered at 90, 180, 270, 360, and 450 seconds. From July 2006 through November 2006, three contrast-enhanced acquisitions were performed with 1.6-mm slice thickness, 420 × 420 matrix, and three contrast-enhanced acquisitions centered at 90, 270, and 450 seconds. The contrast agent administered was 0.1 mmol/kg of body weight of gadodiamide (Omniscan, GE Healthcare).
DWI was performed after the DCE-MRI acquisition using a diffusion-weighted echo-planar imaging (EPI) sequence with parallel imaging (ASSET, GE Healthcare); reduction factor, 2; 7,000/71.5; number of excitations, 3; matrix, 192 × 192; field of view, 36 cm; slice thickness, 5 mm; and gap, 0. Diffusion gradients were applied in six directions with b = 0 and 600 s/mm2, and the scanning time was 2 minutes 40 seconds. It has been shown that the b-value that provides the highest signal-to-noise ratio for a spin-echo diffusion-weighting sequence is equal to 1.1 / ADC [24]. For breast imaging, with typical reported ADC values of 1.6–2.0 × 10–3 mm2/s for normal tissue, this corresponds to an optimal diffusion weighting of approximately b = 600 s/mm2.
Image Analysis
DCE-MRI scans were prospectively interpreted by one of four fellowship-trained radiologists specializing in breast imaging, all with breast MRI experience. Each lesion was assessed using the American College of Radiology BI-RADS breast MRI lexicon incorporating morphologic and kinetic features. Lesion characteristics, including size and location, as well as the BI-RADS assessment and recommendation were recorded at the time of interpretation. This information was entered into our clinical database along with detailed histopathology for each lesion and was later extracted for the purposes of this study. Because the DCE-MRI scans were evaluated prospectively, the radiologists were blinded to lesion outcomes at the time of interpretation.
The diffusion-weighted images were not interpreted at the time of the initial clinical evaluation and were analyzed retrospectively for this study by researchers blinded to lesion outcomes at the time of image analysis. In most cases, correlation between the initial suspicious DCE-MRI finding and the DWI region of interest (ROI) was performed by an MRI physicist with 12 years of experience in breast MRI who was assisted by a resident physician and two student researchers. Ambiguous cases (in which more than one enhancing lesion was present on DCE-MRI or the report was unclear) were reviewed with a radiologist specializing in breast imaging and breast MRI for final consensus.
Images were spatially registered using a nonlinear-based registration algorithm (CADstream, Confirma) to correct for patient motion and eddy current–induced image distortion. The b = 0 s/mm2 images were used as a reference to register the corresponding b = 600 s/mm2 diffusion-weighted images. Diffusion maps were created using in-house Java-based software (Sun Micro-systems) incorporating ImageJ (National Institutes of Health, public domain) and JDTI (Daniel P. Barboriak Laboratory, Duke University School of Medicine) image processing tools. A noise-level threshold of 200 was applied to mask the b = 0 s/mm2 images before creating diffusion maps. ADC maps were created from the spatially registered diffusion weighted images bywhere SDWI is the combined DWI (geometric average of individual b = 600 s/mm2 diffusion-weighted images), and S0 is the b = 0 s/mm2 reference image.
\[ADC=-\frac{1}{b}\mathrm{ln}\left(\frac{S_{DWI}}{S_{0}}\right)\]
An ROI was defined for each DCE-MRI–detected lesion at the corresponding location on the combined DWI (SDWI) series. The ROI was drawn freehand to include the area of hyperintensity and encompass as much of the abnormality as possible while staying within the border of the hyperintense region. Care was taken to avoid regions of high T2 within a lesion, such as cyst, hematoma, or necrosis, by verifying the ROI against the T2-weighted b = 0 s/mm2 image. When a lesion was not hyperintense on DWI, the ROI was drawn at the corresponding location and size as reflected on DCE-MRI. The mean ADC of the voxels in the ROI was calculated for each lesion.
Statistical Analysis
Mean ADC values for benign lesions, DCIS, and invasive carcinomas were compared by generalized estimating equations (GEEs), analogous to a Student's t test with sandwich standard errors to adjust for multiple lesions per patient [25]. All tests were two-sided. PPV was defined as the proportion of biopsied lesions that were diagnosed with breast cancer, designated as PPV3 in the BI-RADS guidelines [23]. PPV was computed for DCE-MRI alone (based on biopsy recommendation) and for DCE-MRI plus DWI (based on biopsy recommendation by DCE-MRI and an ADC threshold value with 100% sensitivity). The 95% CIs for PPV were based on Wilson score binomial 95% CIs and GEEs. Analyses were conducted using R, version 2.5.0 (R Foundation for Statistical Computing) and SAS/STAT software, version 9.1 (SAS Institute).
Results
Of the 83 BI-RADS 4 and 5 lesions in the study, 52 (63%) were benign and 31 (37%) were malignant as determined by tissue sampling. Lesion characteristics are reported in Table 1. Eleven of 31 malignancies were ductal carcinoma in situ (DCIS) and 20 were invasive carcinoma. Lesion sizes, as defined by the longest dimension on DCE-MRI, ranged from 0.4 to 8.3 cm (median, 1.2 cm). Lesion types included two foci (both DCIS), 47 masses (31 benign, 15 invasive carcinoma, and one DCIS), and 34 nonmasslike enhancement (21 benign, five invasive carcinoma, and eight DCIS).
| Characteristic | No. of Lesions | % |
|---|---|---|
| Sizea (cm) | ||
| ≤ 1 | 34 | 41 |
| 1.1-2 | 16 | 19 |
| > 2 | 33 | 40 |
| Type | ||
| Focus | 2 | 2 |
| Mass | 47 | 57 |
| Nonmasslike enhancement | 34 | 41 |
| Histology | ||
| Malignant lesions (all) | 31 | 37 |
| Ductal carcinoma in situ | 11 | 13 |
| Invasive ductal carcinoma | 15 | 18 |
| Invasive lobular carcinoma | 5 | 6 |
| Benign lesions (all) | 52 | 63 |
| Fibroadenoma | 8 | 10 |
| Pseudoangiomatous stromal hyperplasia | 6 | 7 |
| Atypical ductal hyperplasiab | 5 | 6 |
| Fibrocystic | 5 | 6 |
| Focal fibrosis | 5 | 6 |
| Normal breast tissue | 5 | 6 |
| Adenosis | 3 | 4 |
| Papilloma | 3 | 4 |
| Atypical lobular hyperplasia | 2 | 2 |
| Inflammation | 2 | 2 |
| Sclerosing adenosis | 2 | 2 |
| Apocrine metaplasia, fibromatosis, hemangioma, hyperplasia, lobular carcinoma in situ, lymph node | 1 each | 1 each |
a
Size defined as longest diameter on dynamic contrast-enhanced MRI.
b
Not upgraded at excision.
Diffusion-Weighted Imaging Lesion Characteristics
Seventy-seven of 83 suspicious MRI lesions were visible as hyperintense on DWI, including both carcinomas (Fig. 1A, 1B, 1C) and benign lesions (Fig. 2A, 2B, 2C). Six lesions were isointense to surrounding tissue and were not easily identified on DWI. The six isointense lesions ranged in size from 0.5 to 6.4 cm (median, 1.5 cm) on DCE-MRI and included three small masses (each under 1 cm) and three nonmasslike enhancement lesions. Five of the isointense lesions were benign on biopsy (including pseudoangiomatous stromal hyperplasia in two cases, hemangioma, apocrine metaplasia, and normal breast tissue), and one was malignant (0.8-cm invasive ductal carcinoma).
Despite considerable overlap in values between benign and malignant lesions, the 31 malignant lesions exhibited significantly lower mean ADC (1.30 ± 0.27 × 10–3 mm2/s) than the 52 benign lesions (1.70 ± 0.44 × 10–3 mm2/s, p < 0.001) (Table 2). DCIS lesions (mean ADC, 1.31 ± 0.24 × 10–3 mm2/s) were significantly lower in ADC than benign lesions (p < 0.001) but were not significantly different from invasive carcinomas (mean ADC, 1.29 ± 0.29 × 10–3 mm2/s; p = 0.80). No significant difference in ADC was observed between invasive ductal carcinomas (n = 15, mean ADC, 1.29 ± 0.29 × 10–3 mm2/s) and invasive lobular carcinomas (n = 5, mean ADC, 1.29 ± 0.31 × 10–3 mm2/s; p = 0.95).
| Type of Lesion | No. of Lesions (n = 83) | ADC (× 10-3 mm2/s) (Mean ± SD) | ADC Difference From Benign Lesions | pb |
|---|---|---|---|---|
| Benign | 52 | 1.70 ± 0.44 | — | — |
| Malignant (combined)c | 31 | 1.30 ± 0.27 | -0.40 | <0.001 |
| Ductal carcinoma in situ | 11 | 1.31 ± 0.24 | -0.39 | <0.001 |
| Invasive carcinoma | 20 | 1.29 ± 0.29 | -0.41 | <0.001 |
Note—Dash indicates not applicable.
a
Findings of BI-RADS category 4 or 5 at dynamic contrast-enhanced MRI.
b
Fitted average difference from generalized estimating equations, analogous to Student's t test with sandwich standard errors to adjust for multiple lesions in some patients.
c
Includes all carcinomas.
Diagnostic Performance
We evaluated the difference in PPV for lesions recommended for biopsy by breast MRI without and with DWI. The PPV for DCE-MRI alone with BI-RADS 4 and 5 considered positive was 31 of 83 (37%; 95% CI, 28–48%). On DWI, all malignancies (DCIS and invasive carcinoma) had ADC ≤ 1.81 × 10–3 mm2/s (Fig. 3). Applying this ADC threshold to ensure 100% sensitivity, the addition of DWI produced a PPV of 31 of 66 (47%; 95% CI, 35–58%). With the ADC cutoff chosen for 100% sensitivity, the negative predictive value (NPV) was, by definition, also 100%. To account for multiple lesions in the same patient, the PPV was also computed using GEEs with exchangeable correlation. The estimated PPV and 95% CIs with this alternative analysis did not differ by more than a few percentage points. Applying the ADC threshold of 1.81 × 10–3 mm2/s, the improvement in PPV was similar for masses (PPV = 46% vs 35% for DCE-MRI alone) and nonmasslike enhancement (PPV = 45% vs 38% for DCE-MRI alone). Stratified by lesion size, the improvement in PPV was more pronounced for smaller (≤ 1 cm) lesions, such as that shown in Figure 4A, 4B, 4C, in which PPV = 52% versus 35% for DCE-MRI alone, compared with lesions > 1 cm (PPV = 44% vs 39% for DCE-MRI alone).
Many benign lesions exhibited ADC values below the cutoff and were suspicious on both DCE-MRI and DWI. An example of such a false-positive finding is shown in Figure 5A, 5B, 5C. Nevertheless, if biopsy had been recommended for only those suspicious lesions on DCE-MRI with ADC below 1.81 × 10–3 mm2/s, biopsy might have been avoided for 17 (33%) of 52 benign lesions and no cancers would have been missed.
Discussion
Our findings show that for suspicious breast lesions detected initially by MRI and recommended for biopsy (BI-RADS 4 or 5), malignancies exhibit significantly lower mean ADC values compared with benign lesions, and increased PPV can be achieved by incorporating an ADC threshold into the breast MRI assessment. To our knowledge, this is the first study to show the added diagnostic value of DWI as an adjunct to conventional breast MRI for improving PPV. Although previous studies have shown promising differences in ADC between benign and malignant breast lesions [12–19] and high diagnostic accuracy through a multivariate combination of ADC and DCE-MRI features [22], no studies have compared the diagnostic performance of breast MRI with and without DWI.
The mean ADC for malignancies in our study was 1.30 ± 0.327 × 10–3 mm2/s and for benign lesions was 1.70 ± 0.44 × 10–3 mm2/s, which compares well with prior reports [13, 19] despite differences in study design. All malignancies in our study were below an ADC threshold of 1.81 × 10–3 mm2/s. Applying this threshold could have prevented biopsy in 17 (33%) of 52 benign lesions. Our results further suggest that the diagnostic performance of DWI is similar for mass and nonmasslike enhancement type lesions and may be higher for smaller (≤ 1 cm) versus larger lesions. These findings show promise for using DWI to improve the PPV of breast MRI, particularly for more challenging cases (such as small lesions and nonmasslike enhancement), warranting the need for further investigation and validation in larger studies.
One of the malignancies was isointense on DWI, suggesting that DWI may have lower sensitivity than DCE-MRI for detecting breast cancer. This has been described previously, with 6–37.5% of malignant breast lesions reportedly not visible on DWI [14, 26, 27]. As an adjunct tool for breast MRI assessment, it is important to localize the ADC measurement on the basis of the DCE-MRI abnormality to avoid missing any cancers.
DWI is a short unenhanced scan that can be inserted easily into standard clinical breast MRI protocols, but there are challenges for measuring the ADC of breast lesions. Our investigation found that DWI scans for 11 (11%) of 98 lesions exhibited misregistration between the b = 0 s/mm2 image and the individual diffusion-weighted b = 600 s/mm2 images that could not be corrected by the spatial registration algorithm applied in postprocessing. Even with a fast “motion-freezing” EPI imaging technique, bulk patient motion can result in misregistration between the different acquisitions. Also, eddy current–based distortions are common artifacts in diffusion-weighted EPI sequences [28] and are another potential source of spatial misregistration in breast DWI. Misregistration between the diffusion-weighted images was observed to produce substantial errors in ADC calculation in some cases, as has been reported previously [17, 18, 28].
Improving patient comfort to reduce motion, respiratory gating, and alternative pulse sequences or postprocessing techniques to reduce eddy current–based distortions may help to improve the quality of clinical breast DWI data [28–30]. Another challenge to be considered for measuring ADC of suspicious breast lesions is the geometric distortion inherent to EPI images because of low bandwidth in the phase-encoding direction [28]. Although parallel imaging techniques can minimize this distortion, direct voxel-by-voxel comparison between T1-weighted DCE-MR images and diffusion-weighted EPI images remains difficult.
Although our retrospective study did not assess the impact on reading times of adding DWI to the breast MRI examination, it is anticipated to be relatively low. ADC maps can be generated directly by most MRI scanners to be available at the time of reading. Furthermore, the development of diagnostically meaningful ADC thresholds will enable faster interpretation through more informative ADC color maps.
There are limitations to our study. Our imaging was performed at 1.5 T and DWI was acquired with relatively thick slices (5 mm) for signal-to-noise ratio purposes. Partial volume averaging within imaging slices may have contributed to the lack of visibility of a number of lesions on DWI. Longer DWI scanning times may be necessary to increase the signal-to-noise ratio and allow a decrease in slice thickness. Scanning at a higher field strength may also enable a DWI acquisition with thinner slices and better show small or diffuse lesions, as recently shown at 3 T [31]. In vivo ADC measures are influenced by the degree of diffusion sensitization (b-value) applied during DWI acquisition [32], therefore the ADC ranges for benign and malignant lesions obtained in our study at b = 600 s/mm2 may not be the same for DWI obtained at higher or lower b-values. Furthermore, the ADC threshold we used to assess the added diagnostic value of DWI was calculated using available data, whereas the DCE-MRI threshold was based on external (BI-RADS) criteria. DWI was performed approximately 10 minutes after injection of a gadolinium-based contrast agent during DCE-MRI. Although several prior studies have shown no significant effect on ADC after administration of a gadolinium-based contrast agent [16, 33–35], it may be preferable to acquire the DWI sequence before contrast injection to avoid any confounding effects.
In summary, we found that in a group of suspicious breast lesions detected by DCE-MRI and recommended for biopsy, carcinomas exhibited lower mean ADC compared with benign lesions. Adding an ADC threshold to the breast MRI assessment increased the PPV over DCE-MRI alone and would have prevented biopsy for 33% of benign lesions. The improvement in PPV by DWI was not found to be limited by lesion type or size. However, because of considerable overlap in ADC of benign and malignant lesions, breast DWI must remain as a research tool until larger studies are performed to validate these findings. Future work is also necessary to assess whether DWI can be used prospectively in combination with DCE-MRI to reduce the number of unnecessary biopsies performed as a result of breast MRI.
Footnotes
Address correspondence to S. C. Partridge ([email protected]).
Supported by grant BCTR0600618 from Susan G. Komen for the Cure and the Avon Breast Cancer Crusade Opportunity Fund.
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Submitted: November 19, 2008
Accepted: June 16, 2009
First published: November 23, 2012
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