Furthermore, in diffusion-MRI studies, a time- and site-dependency of MR scanner system performance can introduce bias in diffusion-MRI measurements, increase the variance of measured diffusion indices and substantially reduce the power of statistical inference for detecting group differences . In this context, a number of in vivo studies have analyzed intra-scanner variability of diffusion-MRI measurements of the brain  ,  ,  — . Moreover, given that the integration of multicenter data would greatly improve the sensitivity of diffusion-MRI studies, recent clinical investigations have specifically evaluated the inter-scanner reproducibility of measurements of different diffusion-tensor imaging DTI -derived indices in the human brain  — .
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In diffusion-MRI of the body, some in vivo studies have evaluated the inter-scan reproducibility of measurements of diffusion indices of the abdomen  —  , liver  —  , prostate  , anal canal  and kidney . However, so far, only a few clinical studies  —  have specifically investigated the reliability of diffusion-MRI measurements in the breast in terms of inter-scan reproducibility as well as intra- and inter-observer reproducibility.
In view of the fact that breast imaging represents a relatively recent field of application of quantitative diffusion-MRI techniques, and based on the importance of guaranteeing and assessing its reliability in clinical as well as research investigations, the aim of this study was to specifically characterize how the main MR scanner system-related factors affect quantitative measurements in diffusion-MRI of the breast.
In particular, we evaluated the accuracy, inter-scan and inter-scanner reproducibility of measurements of phantom diffusion indices performed on 1. All diffusion-MRI acquisitions were performed on three commercial 1. All MR scanner systems were equipped with a dedicated multi-channel breast coil with 8, 7 and 4 elements for scanner-A, scanner-B and scanner-C, respectively.
For each MR scanner system, standard maintenance and quality assurance procedures were routinely performed. The same doped per g H 2 O distilled: 1. Images from different MR scanner systems were obtained using pulse sequences provided by the manufacturers.
For diffusion-weighted image acquisition, we used a 2D axial spin echo - echo planar imaging sequence, sensitized to diffusion DWI-SE-EPI through strong magnetic field gradient pulses. The acquisition protocols and parameters are reported in Table 1.
For each MR scanner system, all acquisitions were performed on the same day in order to avoid any mid- and long-term changes in scanner performance as well as any potential variability induced by phantom repositioning. The phantom i. The centre of each of the two cylindrical bottles was placed in the centre of each of the two sides of the breast coil and secured using foam padding.
The central slice of the acquisition slab 21 slices was placed at the centre of the two bottles Figure 1. The temperature of the scanner bore was recorded during data acquisition.
The above acquisitions were repeated obtaining a total of 5 measurements. In particular, for each MR scanner system, we used an analytical equation derived by fitting experimental water diffusion coefficients measured at different temperature values with the Arrhenius activation law to obtain the true phantom diffusion coefficient at T a D a . The SNR was calculated using non-diffusion-weighted b 0 images. Conventional approaches to evaluate SNR are based on the signal statistics in one or two separate large regions of interest of a single image or the signal statistics in a large region of interest of a difference image of two repeated acquisitions  , .
Furthermore, the overall percent coefficient of variation for repeated measurements of ADC along the i th diffusion weighting direction was computed as follows: 2. The spatial non-uniformity levels of maps of ADC along each of the main orthogonal directions were evaluated by adapting a method proposed by Magnusson and Olsson . Then, the mean value C within ROI ref was estimated. Finally, for each diffusion weighting direction, the overall non-uniformity degree was estimated as the mean of across repetitions.
In order to estimate the diffusion tensor, we adopted a method similar to that described in previous breast DTI studies  , . Any significant difference in quality control data and measured diffusion metrics, both across the main orthogonal directions within a single MR scanner system and across MR scanner systems, was assessed through a one-way analysis of variance ANOVA. The one-sample t-test, with Bonferroni correction for multiple comparisons, was used to evaluate any significant difference between the true diffusion indices and estimated diffusion indices.
The dashed line represents the known phantom diffusion coefficient 2. A number of in vivo studies have evaluated the reliability of diffusion-MRI measurements in the brain as well as body  ,  ,  —  , .
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However, a more specific and careful evaluation of the reliability of diffusion-MRI measurements of the breast would be of practical interest. Recently, O'Flynn et al. Partridge et al. Tagliafico et al. Additionally, when measuring ADC at 1. It should be noted that assessing and guaranteeing reliability of quantitative diffusion-MRI measurements, which is a prerequisite for successful clinical as well as research studies, necessarily includes a characterization of the MR scanner system.
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Indeed, although in vivo studies can evaluate repeatability and reproducibility of diffusion-MRI measurements in a clinical setting which are fundamental elements toward carrying out longitudinal as well as multicenter studies , such studies do not allow to address measurement accuracy as well as some of the main characteristics of MR scanner system e. A limited number of studies have reported phantom data specific to the characterization of MR scanner systems for diffusion-MRI of the brain as well as the body  —  ,  ,  ,  ,  , .
However, in diffusion-MRI of the breast, only a few clinical studies have incorporated a basic verification of the calibration of diffusion gradients  ,  ,  ,  , . To the best of our knowledge, this is the first phantom study which carries out multiple and specific quality controls in order to characterize in detail different 1.
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In particular, for each MR scanner system, we evaluated the calibration of high strength diffusion gradients for the three main orthogonal axes along which diffusion-sensitizing gradients can be applied. We used acquisition protocols and parameters typically employed in diffusion-MRI of the breast, which, except for small differences in readout bandwidth BW values, were similar for all MR scanner systems. As suggested by Bogner et al.
For all acquisitions, we used the same homogeneous and isotropic phantom with known diffusion coefficient, allowing a proper evaluation of the accuracy of estimated diffusion indices as well as non-uniformity of maps of diffusion indices. In this context, as previously described by Delakis et al.
In particular, both precision and accuracy of diffusion indices can depend on SNR  —  ,  ,  — . Therefore, SNR results cannot be ascribed to differences in BW values only, and are likely to also reflect different overall sensitivities of the breast coils. All MR scanner systems showed a high short term stability of the performance of diffusion gradients.
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For each MR scanner system, the overall coefficient of variation for repeated measurements of ADC along each of the main orthogonal directions was less than 1. Moreover, for each MR scanner system, the entity of this difference varied significantly with diffusion direction Figure 2. This effect, when quantified in terms of the coefficient of variation of ADC measurements across the main orthogonal directions, was more relevant for scanner-A 7. As a whole, these results indicate a mismatch between the theoretically assumed and the effective b-value.
This could originate from errors in diffusion gradients amplitude, eddy current fields, concomitant field terms and cross terms between diffusion gradients and imaging gradients  ,  ,  ,  , . These factors are direction-dependent and can have deleterious effects that are more prominent at the high gradient strengths usually employed in diffusion-MRI  , .
In addition, any diffusion gradient non-uniformity is expected to yield a spatial variation in measured diffusion indices. For each MR scanner system, we observed that the spatial non-uniformity values of maps of ADC along each of the main orthogonal directions depended significantly on the diffusion weighting direction.
Scanner-A showed a relatively high spatial non-uniformity value 7. In general, when DWI-SE-EPI sequences Table 1 are acquired, the high strength diffusion gradients system belonging to each MR scanner system presented an overall mis-calibration not documented by standard maintenance procedures and quality assurance routines , which can affect diffusion indices measurement. Therefore, in order to improve the reliability of quantitative diffusion-MRI of the breast, suitable correction methods could be employed  ,  ,  , .
The greater experimental variability of in vivo diffusion-MRI measurements when compared to our phantom study is likely due to patient repositioning, manual ROI positioning and motion induced effects. This indicates a correct pulse timing when using multiple oblique diffusion gradients as employed in DTI, and may suggest the negligibility of cross-term effects between diffusion and imaging gradients along different directions  ,  , . Therefore, a comparison of breast diffusion-MRI data from different centers should be performed with great caution.
Moreover, during the planning of a multicenter study, the accuracy of diffusion-MRI measurements should be carefully assessed in every participating center.
Additionally, in longitudinal studies, a periodic monitoring of the accuracy of measured diffusion indices is highly recommended. In a meta-analysis of 13 studies dealing with quantitative diffusion-MRI in the differential diagnosis of breast lesions, Chen et al. This heterogeneity could be due to differences in patient characteristics and diagnostic criteria, as well as to different diffusion-MRI acquisition and analysis methods. However, we hypothesize that potential differences in MR scanner system-related factors between different MR scanner systems, which can systematically bias accuracy and precision of diffusion-MRI measurements, may contribute to explaining the results heterogeneity reported by Chen et al.
While for each MR scanner system FA values were less than 0. Although breast imaging is an appealing and promising application field of diffusion-MRI, only few in vivo studies have recently evaluated the inter-scan reproducibility as well as intra- and inter-observer reproducibility of diffusion measurements of the breast  — . In this phantom study, we characterized in detail three 1. The SNR as well as overall calibration of high strength diffusion gradients system varied substantially across MR scanner systems, introducing systematic bias in measurements of diffusion indices.
We note that in vivo diffusion-MRI measurements of the breast can also depend on other non-MR scanner system-related factors — such as subject-related artifacts e.