 Research
 Open Access
Automated analysis of nonmassenhancing lesions in breast MRI based on morphological, kinetic, and spatiotemporal moments and joint segmentationmotion compensation technique
 Sebastian Hoffmann^{1},
 Jamie D Shutler^{2},
 Marc Lobbes^{3},
 Bernhard Burgeth^{1} and
 Anke MeyerBäse^{4, 5}Email author
https://doi.org/10.1186/168761802013172
© Hoffmann et al.; licensee Springer. 2013
Received: 15 February 2013
Accepted: 24 July 2013
Published: 15 November 2013
Abstract
Dynamic contrastenhanced magnetic resonance imaging (DCEMRI) represents an established method for the detection and diagnosis of breast lesions. While masslike enhancing lesions can be easily categorized according to the Breast Imaging Reporting and Data System (BIRADS) MRI lexicon, a majority of diagnostically challenging lesions, the so called nonmasslike enhancing lesions, remain both qualitatively as well as quantitatively difficult to analyze. Thus, the evaluation of kinetic and/or morphological characteristics of nonmasses represents a challenging task for an automated analysis and is of crucial importance for advancing current computeraided diagnosis (CAD) systems. Compared to the wellcharacterized massenhancing lesions, nonmasses have no welldefined and blurred tumor borders and a kinetic behavior that is not easily generalizable and thus discriminative for malignant and benign nonmasses. To overcome these difficulties and pave the way for novel CAD systems for nonmasses, we will evaluate several kinetic and morphological descriptors separately and a novel technique, the Zernike velocity moments, to capture the joint spatiotemporal behavior of these lesions, and additionally consider the impact of nonrigid motion compensation on a correct diagnosis.
Keywords
1 Introduction
Breast cancer is one of the leading causes of death among women in the western hemisphere. Contrastenhanced magnetic resonance imaging (MRI) of the breast was reported to be a highly sensitive method for the detection of invasive breast cancer[1]. Different investigators described that certain dynamic signal intensity (SI) characteristics (rapid and intense contrast enhancement followed by a washout phase) obtained in dynamic studies are a strong indicator for malignancy[2]. Morphological criteria have also been identified as valuable diagnostic tools[3]. Recently, combinations of different dynamic and morphological characteristics have been reported[4, 5] that can reach diagnostic sensitivities up to 97% and specificities up to 76.5%. Many of these studies were performed in the preoperative staging of patients with suspicious lesions (Breast Imaging Reporting and Data System (BIRADS) 4 and 5) including predominantly tumors with an extension greater than 2 cm. In such cases, MRI reaches a very high sensitivity in the detection of invasive breast cancer due to both the typical appearance (illdefined shape, stellate borders, and rim enhancement) of malignant tumors and characteristic SI time courses of contrast enhancement. Recent clinical research has shown that ductal carcinoma in situ (DCIS) with small invasive carcinoma can be adequately visualized in MRI[6] and that MRI provides an accurate estimation of invasive breast cancer tumor size, especially in tumors of 2 cm or smaller[7].
However, more than 40% of the falsenegative MR diagnosis are associated with nonmasslike enhancing lesions, thus indicating a lower sensitivity of MRI for these cases. It has been shown that double reading achieves a higher sensitivity but is timeconsuming, and as an alternative, a computerassisted system was suggested[8]. The success of computeraided diagnosis (CAD) in conventional Xray mammography[9–13] motivates furthermore the research of similar automated diagnosis techniques in breast MRI.
Nonmassenhancing lesions exhibit a heterogeneous appearance in breast MRI with high variations in kinetic characteristics and typical morphological parameters[14–16] and have a lower reported specificity and sensitivity than massenhancing lesions. The diagnosis of nonmasslike enhancement lesions is thus far more challenging. Malignant lesions such as DCIS and invasive lobular cancer (ILC) exhibit a segmental or linear enhancement pattern, and benign lesions such as fibrocystic changes present as well a nonmasslike enhancement[17]. However, a systematic classification of nonmasslike enhancing lesions is not in place. A classification of such lesions would be highly beneficial since they may reduce the biopsies’ numbers. The morphological parameters with the highest predictive value in nonmassenhancing lesions were reported in[15] as segmental distribution, clustered ring enhancement, and a clumped internal architecture. Another study has shown that including kinetic data on dynamic contrastenhanced imaging and diffusionweighted MRI imaging in addition to morphological characteristics showed a high diagnostic accuracy in the characterization of these lesions[16].
Research initiatives have been focused on automated analysis of mass lesions[18–24], while very few studies investigated the characterization of the morphology and/or enhancement kinetic features of nonmass lesions[17, 25–27]. The studies showed a much lower sensitivity and specificity for nonmasslike enhancement lesions compared with masses and suggested the need for more advanced algorithms for the diagnosis of nonmasslike enhancement.
Current CAD systems are specialized for automated detection and diagnosis of massenhancing lesions that are well characterized by shape and kinetic descriptors according to the BIRADS lexicon. To overcome these problems and revolutionize the state of the art of CAD in breast MRI, we need to focus on correctly capturing and analyzing the unique spatiotemporal behavior of nonmassenhancing lesions.
In this paper, we present novel techniques for establishing the automated diagnosis of nonmassenhancing lesions and thus improve the quality of breast MRI postprocessing and reduce the number of missed or misinterpreted cases leading to falsenegative diagnosis. In an automated step, we will extract both morphological and kinetic features and use them as potential cues for nonstandard lesion detection. Furthermore, we will apply a novel concept  the Zernike velocity moments[28]  as a unique descriptor that captures the simultaneous behavior of the spatiotemporal behavior of these lesions. We will evaluate quantitatively and qualitatively based on automated classification the utility of novel feature extraction approaches to diagnostically challenging lesions in breast MRI.
2 Materials and methods
2.1 Patients
The database for nonmassenhancing lesions includes a total of 84 patient images, all female, with nonmassenhancing tumors. All patients had a histopathologically confirmed diagnosis from needle aspiration/excision biopsy and surgical removal. Histologic findings were malignant in 61 and benign in 23 lesions.
2.2 MR imaging
MRI was performed with a 1.5 T system (Magnetom Vision, Siemens, Erlangen, Germany) equipped with a dedicated surface coil to enable simultaneous imaging of both breasts for both types of lesions. The patients were placed in a prone position.
Transversal images were acquired with a short TI inversion recovery (STIR) sequence (TR = 5,600 ms, TE = 60 ms, FA = 90°, IT = 150 ms, matrix size 228 × 182 pixels, slice thickness 3 mm). Then, a dynamic T1weighted gradient echo sequence (3D fast lowangle shot sequence) was performed (TR = 4.9 ms, TE = 1.83 ms, FA = 12°) in transversal slice orientation with a matrix size of 352 × 352 pixels and an effective slice thickness of 1 mm. The dynamic study consisted of five measurements with an interval of 1.4 min. The first frame was acquired before injection of paramagnetic contrast agent (gadopentatate dimeglumine, 0.1 mmol/kg body weight, Magnevist^{ TM }, Schering, Berlin, Germany) immediately followed by the four other measurements.
2.3 Motion compensation and lesion segmentation
Automatic motion correction represents an important prerequisite to a correct automated small lesion evaluation[29]. Motion artifacts are caused either by the relaxation of the pectoral muscle or involuntary patient motion and invalidate the assumption of same spatial location within the breast of the corresponding voxels in the acquired volumes for assessing lesion enhancement. We employ a motion compensation algorithm based on the technique described in[30] and use separate robustification in the data term. It has been shown that this method yields very good results as it is robust against noise, which is very important for our purposes.
Tumor segmentation represents the correct identification of the spatial location of a tumor. Manual segmentation performed by a radiologist is considered the gold standard. However, expert segmentation is not highly precise and prone to interobserver and intraobserver variability, and it might include also nonenhancing tissue. It is timeconsuming by viewing both spatial and temporal profiles and thus examining many series of enhanced data and profiles of pixels while determining the lesion boundary. To overcome these problems, we employ as an automatic segmentation method an active contour segmentation without edges as proposed by Chan and Vese[31] and improve the algorithm by taking into account the threedimensional image sequence and by adding a smoothness assumption to level set function:
where {f _{ d }}_{ d = 1,..,n } is the image sequence for a given case consisting of n threedimensional images. In our case, n = 5.${c}^{\text{in}}={({c}_{1}^{\text{in}},\dots ,{c}_{n}^{\text{in}})}^{T}$ are the average gray values for each image for the inside region, and similarly,${c}^{\text{out}}=({c}_{1}^{\text{out}},\dots ,{c}_{n}^{\text{out}})$ for the outside region. Since the contrast agent has a certain intaketime, the consecutive images will be weighted more. The weighting factors γ _{1},…,γ _{ n } ≥ 0 take into consideration accordingly this information content of an image. We also use${\delta}_{\epsilon}(x):=\frac{1}{2}\left(1+\frac{2}{\pi}\phantom{\rule{.3em}{0ex}}arctan\phantom{\rule{.3em}{0ex}}\left(\frac{x}{\epsilon}\right)\right)$, n := outer normal direction of ∂ Ω, and scalar parameters μ, λ _{1}, λ _{2}.
where τ is the tolerance. To get a good approximation of a global optimizer of this nonconvex problem, we make use of a coarsetofine multigrid implementation of the algorithm. The parameter η ∈ [0.5,1) thereby determines the downsampling factor.
3 Enhancement kinetic features
While massenhancing lesions exhibit a typical kinetic behavior that is distinctive for malignant and benign lesions, nonmassenhancing lesions have kinetic characteristics that are far less well characterized and of limited accuracy in discriminating between malignant and benign behavior[26]. As a dynamical feature, the slope of the relative signal intensity enhancement (RSIE) is used in most current CAD systems. Very few studies exist for analyzing the kinetics of nonmasses.
Besides the description of the texture, we also want to characterize the enhancement of the tumor due to the contrast agent. We are focusing on this in the following mainly by considering the mean gray values of each tumor region and how it develops over time. Therefore, we consider trivial facts like the magnitude of the enhancement as well as more sophisticated methods like the Fourier transform or regression methods. All these approaches are described in the following.
3.1 Slope of mean values
where Δt denotes the time between the images. We take these values as additional features. This is the same as computing the average of all slopes between single pixels.
3.2 Regression methods
Given the points {(t _{ i },s _{ i })^{⊤}}_{ i=1,…,I } with t _{ i } = i Δt, we to try apply regression with different functions described below.
3.2.1 Linear function
This feature is also known as the relative signal intensity enhancement and was already used by Retter and Steinbrücker for masslike tumors[32–34]. The idea behind it is that in the beginning, both benign and malignant tumors have the same behavior by absorbing a lot of the contrast agent leading to a rapid enhancement. However, the temporal behavior can be highly diagnostic for the type of the tumor. While benign mass tumors tend to have a further increase of the enhancement, malignant tumors are prone to have a rapid washout effect. The question is if this idea can be transferred to the nonmasslike tumors. Jansen et al. found out in their experiments that this criteria is not valid anymore in this case[35]. However, we want to examine if it is also the case for our data set, and therefore, we are incorporating this feature in the classification process, too.
3.2.2 Exponential function
with the parameters A, α, and β. An example of the fitted function can be seen in Figure3. It is now possible to fit the values instead of approximating them as it is the case with linear functions. The parameters of the nonlinear fitting function can be gained using an iterative algorithm. We used the NelderMead method[36], which is already implemented in Matlab®;. Having these values, Jansen et al. proposed to compute some properties based on the function as features:

Initial area under the curve until a specified time τ. We use τ = 3Δt for our experiments.$\text{iAUC}=A\xb7\left(\frac{1{e}^{\beta \tau}}{\beta}+\frac{{e}^{(\alpha +\beta )\tau}1}{\alpha +\beta}\right)$

Initial slope$\text{iSlope}=\mathrm{A\alpha}$

Time to peak enhancement${\mathrm{T}}_{\text{peak}}=\frac{1}{\alpha log(1+\frac{\alpha}{\beta})}$

Curvature at the peak${\kappa}_{\text{peak}}=A\alpha \beta $
In contrast to the original paper of Jansen et al., we also include the parameters A, α, and β in the feature list.
4 Morphological features
Morphological characteristics contain valuable information about a lesion’s type. Combined with kinetic properties, one could expect a higher accuracy. Furthermore, nonmassenhancing lesions such as DCIS or ICS can be better differentiated based on morphological properties[25]. In a previous work[37], we have considered features that describe the geometric characteristics of the shape and local moments such as Krawtchouk to identify the nonsmooth surface.
In this section, we will focus on features that are solely based on the morphology of the tumor, i.e., we will study the geometric structure without considering the gray values. As a result of the segmentation algorithm, we have a binary image telling us which pixels belong to the tumor and which do not. This representation, however, is not sufficient for our needs. A better representation would be a triangulation of the surface points. This is done using the builtin method in Matlab®;. It uses an edgebased algorithm and returns for a given binary tumor image a set of vertices V consisting of 3D points and faces F defining the triangles connecting the vertices in V. Based on this representation, we can compute the following features.
4.1 Writhe number
The value Δp ^{ ′ } is the area assigned to the point p ^{ ′ }.
The normal of each vertex is then computed by averaging the normals of the faces containing the vertex. Similarly, to obtain a measurement of the value Δp of a vertex p, the areas of the faces containg p are averaged. Having these values, we can compute the writhe number for every vertex. Finally, we compute the firstorder statistics of the values.
4.2 Krawtchouk moments
Krawtchouk moments represent a set of orthonormal polynomials associated with the binomial distribution. Their mathematical derivation is exemplarily described in[41].
where the image f is represented in the radial polar system. To make them rotationally invariant, one considers the norm of the moments. The function K _{ n } refers to the Krawtchouk polynomial of order n. The notations and detailed mathematical derivations are described in[43].
4.3 Zernike velocity moments
where$\overline{{x}_{i}}$ is the current COM in the x direction, while$\overline{{x}_{i1}}$ is the previous COM in the x direction, and$\overline{{y}_{i}}$ and$\overline{{y}_{i1}}$ are the equivalent values for the y direction. Velocity moments have been previously applied to analyze human motion[28]. Here we use the Zernike velocity moments to describe the breast MRI image sequences. These spatiotemporal moments (or descriptors) allow us to capture the spatial variation of contrast enhancement over time within the image sequence (i.e., they capture the changes in signal intensity and shape between scans).
5 Classification techniques
The following section gives a description of classification methods applied to evaluate the effect of automated classification of diagnostically challenging breast MRI lesions such as foci and nonmassenhancing lesions based on several feature extraction methods.
Let us assume that x describes a Kdimensional feature vector and that there are J classes and N _{ j } samples available in group j. The mean in group j is given by μ _{ j }, and the covariance matrix is given by Σ_{ j }.
As classification techniques, we employ support vector machines (SVM) with different kernels.
5.1 Support vector machines
An additional challenge appears if there is a nonlinear function that separates the variable, since the common approach would fail under these circumstances. Aizerman et al. refined this method by using nonlinear kernel functions instead of the scalar product which maps the variables onto another space[45]. The optimal hyperplane computed corresponds to a nonlinear function in the original feature space.
6 Experimental results
Classifiers employed for lesion classification
Name  Description 

SVM kernel 1  SVM classification with a linear kernel 
SVM kernel 2  SVM classification with a polynomial kernel 
SVM kernel 3  SVM classification with radial basis kernel 
SVM kernel 4  SVM classification with sigmoidal kernel 
A recent study for masslikeenhancing lesions[5] has shown that both morphological and kinetic features outperform spatiotemporal features. The morphological features were the most discriminative, suggesting that the lesion’s morphology  in concordance with clinical practice  determines the further evaluation based on a needle biopsy. Kinetic features, on the other hand, seem to be more discriminative in the case of nonmasslike enhancing lesions followed by the morphological ones.
7 Conclusion
We have implemented and tested the most comprehensive computeraided diagnosis system for nonmassenhancing lesions in the literature consisting of motion compensation, segmentation, and feature extraction and classification. These types of lesions are diagnostically challenging since typical kinetic or morphological descriptors are not known so far. The present paper evaluated the discriminative power of a novel joint spatiotemporal technique, the Zernike velocity moments, versus single kinetic or shape descriptors for the diagnosis of these lesions in combination with or without motion compensation. Motion compensation proved in most cases to be diagnostically relevant. The best discriminative features are based on the dynamical properties of an approximation of the RSIE curve, suggesting that kinetics such as washin and washout parameters plays a key role in correctly diagnosing nonmassenhancing lesions and confirms existing studies. The next best feature set is represented by the Writhe number computed for vertices along the surface of the tumor, describing the surface asymmetries. Intuitively, our results for the Writhe number have shown that the more twisted the surface of a lesion is, the greater the likelihood for malignancy is. The spatiotemporal moments, alone, seem to provide an independent characterization of the tumor, and we suspect that in combination with morphological and kinetic features, they will improve their discriminative power. Future studies will be necessary to evaluate in a large trial the effectiveness of these novel descriptors for nonmassenhancing lesion diagnosis.
Declarations
Acknowledgements
This research was supported in part by NIH grant 5K25CA10679905.
Authors’ Affiliations
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