Elsevier

NeuroImage

Volume 118, September 2015, Pages 13-25
NeuroImage

3D MR ventricle segmentation in pre-term infants with post-hemorrhagic ventricle dilatation (PHVD) using multi-phase geodesic level-sets

https://doi.org/10.1016/j.neuroimage.2015.05.099Get rights and content

Highlights

  • Accurate measurement of neonatal IVH ventricular volume is useful.

  • This paper proposes a multi-region segmentation for ventricle extraction.

  • Multiphase geodesic level-set evolution is combined with multi-atlas registered prior.

  • Validation using hydrocephalus and IVH patients suggested its accuracy.

Abstract

Intraventricular hemorrhage (IVH) or bleed within the cerebral ventricles is a common condition among very low birth weight pre-term neonates. The prognosis for these patients is worsened should they develop progressive ventricular dilatation, i.e., post-hemorrhagic ventricle dilatation (PHVD), which occurs in 10–30% of IVH patients. Accurate measurement of ventricular volume would be valuable information and could be used to predict PHVD and determine whether that specific patient with ventricular dilatation requires treatment. While the monitoring of PHVD in infants is typically done by repeated transfontanell 2D ultrasound (US) and not MRI, once the patient's fontanels have closed around 12–18 months of life, the follow-up patient scans are done by MRI. Manual segmentation of ventricles from MR images is still seen as a gold standard. However, it is extremely time- and labor-consuming, and it also has observer variability. This paper proposes an accurate multiphase geodesic level-set segmentation algorithm for the extraction of the cerebral ventricle system of pre-term PHVD neonates from 3D T1 weighted MR images. The proposed segmentation algorithm makes use of multi-region segmentation technique associated with spatial priors built from a multi-atlas registration scheme. The leave-one-out cross validation with 19 patients with mild enlargement of ventricles and 7 hydrocephalus patients shows that the proposed method is accurate, suggesting that the proposed approach could be potentially used for volumetric and morphological analysis of the ventricle system of IVH neonatal brains in clinical practice.

Introduction

The mild enlargement of the cerebral ventricles, called ventriculomegaly (VM), is often seen in neonates born prematurely with the highest risk population being those born at < 32 weeks gestation or with very low birth weight (< 1500 g). One of the primary non-congenital causes of ventriculomegaly is intraventricular hemorrhage (IVH), which is brain bleeding that occurs in 15–30% of very low birth weight pre-term neonates and is predictive of an adverse neurological outcome (Synnes et al., 2001, Adams-Chapman et al., 2008, Klebermass-Schrehof et al., 2013). Infants with IVH are at risk of developing progressive dilatation of the ventricles, a pathology called hydrocephalus. About 30–50% of infants with a severe IVH develop post-hemorrhagic ventricular dilatation (PHVD) and around 20–40% of those patients will consequently develop hydrocephalus, necessitating to be treated with a permanent ventriculo-peritoneal shunt (Adams-Chapman et al., 2008, Klebermass-Schrehof et al., 2013). Preterm infants are at risk of white matter injury, due to either a unilateral parenchymal hemorrhage or a more diffuse bilateral white matter damage, and the development of PHVD increases the risk of an adverse neurodevelopmental outcome. Around 45–60% of infants with PHVD have marked cognitive impairment (developmental quotient equivalent of less than 70) (Adams-Chapman et al., 2008, Klebermass-Schrehof et al., 2013). Any patient with VM will be followed for 1–2 years, as they are at risk of developing hydrocephalus. However, it is difficult to determine how quickly ventricle dilatation is progressing through currently used qualitative viewing of the MR images. During the follow-up, ultrasound (US) or MR images of their brains are acquired to quantitatively monitor the ventricular size. However, while clinicians have a good sense of what VM looks like compared to normal ventricles, there is little information available on what quantitative volumetric normal ranges are for ventricle volume of the cerebral ventricles in pre-term neonates as they mature, and only a few investigative studies (Haiden et al., 2005, Knickmeyer et al., 2008) have been conducted. In addition, VM is considered to be related to diagnosed anomalies of the central nervous system (CNS) (Guibaud, 2009). Although the sources and outcomes of VM have been extensively investigated (Weisglas-Kuperus et al., 1992, Gaglioti et al., 2005, Breeze et al., 2007, Beeghly et al., 2010), much remains unknown due to its variable etiology, complicated pathophysiology, and poorly understood natural history (Gaglioti et al., 2005, Beeghly et al., 2010). Volumetric analysis based on volumetric and morphological biomarkers of the developing neonatal brain can greatly improve the diagnosis, prognosis, and treatment of VM, which requires a robust and accurate automatic segmentation algorithm.

Previous brain segmentation algorithms have been extensively investigated in adult brain MR images, leading to several successful methods and software packages, such as SPM (Ashburner and Friston, 2005) and FreeSurfer (Fischl et al., 2002).

However, there is limited publicly available software for neonatal brain MR image segmentation. Neonatal brain MR images tend to suffer from high image noise, low tissue contrast, and considerable inter-subject anatomical variability, which make most of the methods used for the adult population not applicable to these images (Gui et al., 2012). Segmentation is even more difficult in infants with IVH as their ventricles contain heterogeneous cerebrospinal fluid (CSF) due to the hemorrhage. Wang et al. (2011) developed a coupled level-set method initialized by convex optimization technique for automatic neonatal MR images. Shi et al. (2010a) built a subject-specific tissue probabilistic atlas to segment longitudinal neonatal brain MR images. Wang et al. (2014a) integrated this probabilistic atlas into a patch-driven level-set framework for more accurate segmentation of neonatal MR images. Three different image sets of preterm infants provided in the NeoBrainS12 study (http://neobrains12.isi.uu.nl) (Isgum et al., 2015) were set up to allow a comparison of 8 brain tissue segmentation methods. The results demonstrated that the participating methods were able to segment all tissue classes well, except myelinated white matter. Even though several methods tend to perform better than others, areas of poor segmentation were common to all methods.

Most of previous work (Gui et al., 2012, Wang et al., 2011, Wang et al., 2014a, Shi et al., 2010a, Isgum et al., 2015) segmented neonatal brain MR images into different brain tissues, such as white matter (WM), gray matter (GM), and CSF, but did not focus on the ventricular system. Moreover, these methods were only validated on high-quality healthy neonate images generated for research purposes only while patients were sedated. Gholipour et al. (2012) developed a ventricle segmentation method of fetal brain MRIs using 13 normal brains and 12 fetuses with mild VM, which is the most similar study to ours. However, unlike the healthy brains and the brains with mild VM, the MR images of neonatal patients with IVH and hydrocephalus used in this study provide greater challenges for segmentation. The poor physical condition of these patients does not allow for a normal acquisition time or patient sedation, leading to a much poorer image quality. Furthermore, heterogeneous CSF with degrading blood products and dilatation of the ventricles cause large brain deformation and drastic inter-subject variations in the anatomy from patient to patient (Fig. 1). The blood clots from IVH are not only in the ventricles, but also at the junction between the ventricles and the brain, and infiltrating the brain creating heterogeneous imaging properties. For some severe cases, the ventricle volume is > 70% of the whole brain compared to < 30% of patients with mild VM, making it much more challenging to capture such large shape variability for most multi-atlas registration-based approaches (Warfield et al., 2004, Aljabar et al., 2009). Although manual segmentation is an option, it is too arduous and time consuming to be clinically feasible. Thus, an accurate and robust automatic cerebral ventricle segmentation algorithm from IVH neonatal MRIs is still highly desirable in clinical practice in order to handle images of poor quality and large shape variability.

In this study, we propose a multi-region segmentation approach for delineating the brain ventricle system of pre-term IVH neonate patients from acquired 3D T1 weighted (T1w) MR images. The proposed algorithm is initialized by non-linearly registering multiple pre-segmented patient images onto the subject image using a duality-based convex optimization registration scheme. A variational time-implicit multiphase geodesic level-sets (MGLS) is then proposed to automatically extract the ventricle system, which incorporates an intensity probability density function (PDF) and a probabilistic labeling map as shape priors generated in the initialization procedure. In particular, the major components of the whole segmentation pipeline are implemented using general-purpose programming on graphics processing units (GPGPU) to obtain a high computational efficiency.

The proposed MGLS algorithm is the extension of a 2015 EMMCVPR paper (Rajchl et al., 2015), which only provided a segmentation framework, and was evaluated on one 3D adult MR image. Compared to the previous version based on classic level sets (Rajchl et al., 2015), the geodesic level-sets (Criminisi et al., 2008) is incorporated into the surface evolution to improve the segmentation accuracy, especially for the hydrocephalus patient images. The improved algorithm has been evaluated on a larger number of patient images. To the best of our knowledge, this paper is the first study focusing on automated ventricle segmentation of pre-term neonatal MR images with VM and hydrocephalus.

Section snippets

Segmentation pipeline

Fig. 2 shows an overview of the proposed segmentation pipeline. An input subject image is first classified into a specified patient group (patients with mild enlarged ventricles or hydrocephalus patients) based on the Bhattacharyya distance (Michailovich et al., 2007) between the background and foreground defined by registered pre-segmented labels. Multiple manually pre-segmented patient images from the specified group are registered to the subject image using affine and deformable registration

Image acquisition

All patients were imaged following a protocol approved by the ethics review board at the University of Western Ontario (REB #100315). After an initial diagnosis of IVH on a clinical 2D US exam, the parents of the patient were approached to enroll their child in the study. Imaging sessions would be canceled if patients were not stable as judged by the attending team and nursing staff. Preterm-born patients with different IVH grades were imaged upon reaching term-equivalent age with a 1.5T Signa

Discussion and conclusion

This paper proposes an accurate solution to a challenging segmentation problem of the pre-term IVH neonatal cerebral ventricle from 3D MR images. The proposed segmentation algorithm makes use of the convex optimization technique associated with spatial shape prior, which is built via a multi-atlas non-linear registration scheme. The proposed segmentation pipeline is used for monitoring the ventricular size of patients with mild ventricle enlargement and hydrocephalus. The experimental results

Acknowledgments

The authors are grateful for the funding support from the Canadian Institutes of Health Research (CIHR) and Academic Medical Organization of Southwestern Ontario (AMOSO).

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