A 26-year-old patient underwent endoscopic third ventriculostomy for the treatment of obstructive hydrocephalus. 3D volume data sets were obtained at 3 T before surgery and three times after surgery. Off-line analysis of individual imaging data (initial linear registration, intensity adjustment, and final nonlinear registration of pre- to postoperative MR images) yielded 3D displacement fields representing the postoperative structural brain change. In principle, such an analysis technique can be used in any clinical follow-up for which careful observation of tissue readjustment is of particular importance

Lindner, D.

Meixensberger, J.

Preul, C.

Tittgemeyer, M.

Trantakis, C.

English

Preul, Christoph

Tittgemeyer, Marc

Lindner, Dirk

Meixensberger, Jürgen

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Quantitative assessment of parenchymal and ventricular readjustment to intracranial pressure relief

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Quantitative Assessment of Parenchymal andVentricular Readjustment to IntracranialPressure ReliefChristoph Preul, Marc Tittgemeyer, Dirk Lindner, Christos Trantakis, and Ju¨rgen MeixensbergerSummary: A 26-year-old patient underwent endoscopicthird ventriculostomy for the treatment of obstructive hy-drocephalus. 3D volume data sets were obtained at 3 Tbefore surgery and three times after surgery. Off-line anal-ysis of individual imaging data (initial linear registration,intensity adjustment, and final nonlinear registration ofpre- to postoperative MR images) yielded 3D displacementfields representing the postoperative structural brainchange. In principle, such an analysis technique can beused in any clinical follow-up for which careful observationof tissue readjustment is of particular importance.The adaptation of the brain parenchyma and ven-tricular system to altered intracranial pressure condi-tions is an important part of the evaluation of MRimages. In the treatment of hydrocephalus, for in-stance, these changes can be vital when comparingpre- and postoperative ventricular size. We introducea technique for visualizing and quantifying the dy-namics of such tissue adaptation.MR imaging provides a standard method in preop-erative diagnostic performance to visualize the mor-phology of the third ventricle and its anatomic land-marks (1–5). The routine procedure of endoscopicthird ventriculostomy bypasses a stenotic aqueduct orfourth ventricular outlet by windowing the third ven-tricular floor to deviate the CSF into the interpedun-cular and prepontine cisterns (5–7). In the postoper-ative course, MR imaging is used to verify the patencyof the stoma and to evaluate any ventricular adjust-ment (8–10). The readjustment of the ventricularsystem is one prominent parameter with which todocument the success of the intervention, aside fromclinical improvement (6, 8, 11).The dynamics of textural and ventricular readjust-ment after intracranial pressure relief has not beenlargely investigated or visualized to date. We moni-tored such structural change by means of off-lineimage processing of subsequent MR images. Thenonlinear mapping of these images onto one anotheryields the displacement vectors that reflect the struc-tural change. A quantification of the displacementvectors can be enlisted as a criterion accompanyingthe clinical course and, thus, can aid in comprehen-sion of the success or failure of the intervention.TechniqueDeformation Field AnalysisTo quantitatively estimate structural reconfiguration, weused a multi-step approach. First, the MR images were reori-ented to the plane of anterior and posterior commissure. Uponreorientation, the images were processed for gray-scale nor-malization and removal of intensity inhomogeneities. Rigidregistration was then applied to align objects in the images forposition and orientation. A fuzzy C means the algorithm wasused to segment the tissue types (12). To assess volumetricvalues for the ventricles, the lateral and third ventricles weresegmented according to the procedure as introduced by Hoj-jatoleslami and Kruggel (13) and adapted by Schnack et al (14).After segmentation, the ventricular and cortical surfaces weregenerated as smooth triangular meshes, where brain substruc-tures such as brain stem and cerebellum have been removed.Non-rigid registration was used to monitor residual differencesbetween the images, which reflect morphologic, local changes.Because of the large deformations that originate from theneurosurgical approach, we based this registration on a fluiddynamic model (15, 16). The resulting vector field was thensuperimposed in a 1:1 size relation to the underlying MR imageto render a direct measurement of change possible (Fig 3).Standard Manual Planimetric Measures of the VentriclesTo assess the ventricular size, we measured a ventricularbody index and the width of the third ventricle. The ventricularbody index is the relation between the maximum distance of thelateral ventricles at the level of the ventricular body and theinternal diameter of the skull at the same level and orientation.The third ventricle was measured at its maximum anteriorwidths.ResultsClinical CaseA 26-year-old man presented to the neurosurgeryclinic with subacute onset of attacks of headaches,vertigo, and nausea but without any focal neurologicdeficits. Preoperative MR imaging revealed a lateraland third ventricular enlargement and showed evi-dence for an at least partially occluded aqueduct,suggesting noncommunicating triventricular hydro-cephalus (Fig 1). Third ventricular bulging pushed theReceived April 10, 2003; accepted after revision August 26.From the Max-Planck-Institute of Human Cognitive and BrainScience (C.P., M.T.) and the Klinik und Poliklinik fu¨r Neuro-chirurgie der Universita¨t Leipzig (C.P., D.L., C.T., J.M.),Leipzig, Germany.Address reprint requests to Christoph Preul, MD, Max-Planck-Institute of Human Cognitive and Brain Sciences, Stephenstrasse1a, 04103 Leipzig, Germany.© American Society of NeuroradiologyAJNR Am J Neuroradiol 25:377–381, March 2004Technical Note377anterior recessus toward the infundibular fossa. Brainstem and pontine structures bent toward the clivus. Theendoscopic procedure was performed through a rightside paramedian coronal burr hole by using a rigidneuroendoscope. In situ inspection showed turbulentCSF flow between the third ventricular floor and theinterpeduncular cistern after windowing the terminalmembrane and a firm additional membrane underneaththe real third ventricular floor. The patient totally re-covered from his symptoms shortly after surgery.Figure 1 shows the preoperative condition and thelatest postoperative condition. The postoperative MRimages were obtained 4 days, 3 months, and 8 monthsafter the intervention and show readjustment of theventricles and brain tissue to the altered intracranialpressure condition (Fig 2). Regarding the ventricularsystem, deformation analyses revealed an upward move-ment of the pontine and brain stem structures of 9 mm.The third ventricular floor, especially the terminal mem-brane, retreated from the infundibular recess for 5 mm.In addition, the whole ventricular roof descended 8.5mm (Fig 3B and C). Planimetric measurement revealeda constant decrease of the ventricular body index andthe third ventricular widths from 0.47 to 0.38 and from19 mm to 12 mm, respectively. These values highlycorrelate with r  0.968. The volume of the ventricles(lateral ventricles plus third ventricle) decreased by 49%from the preoperative to the latest postoperative MRimage. Figure 2 suggests a continuous decrease of allventricular compartments.Figure 3 substantiates the underlying local shapedifferences in a color-coded visualization: for eachpoint on the ventricular surface (Fig 3A) or brainsurface (Fig 3B), the displacement vector is decom-posed into its two components. One is perpendicular(normal) and the other tangential to the surface. Ifthe normal component points inward, the shape dif-ference is coded in red; conversely, the blue colorcorresponds to outward-pointing normals. The inten-sity of the respective color reflects the magnitude ofthe underlying displacement vector. The scale is pre-sented in millimeters.Additionally, a sparse set of the displacement vec-tors themselves is shown as arrows (with green stem,purple basis, and yellow arrowhead). Because thedisplacement vectors are defined at any voxel in theimage volume, morphologic change can be visualizedat any location within the brain. The capability of thevector field analysis is impressively shown at the thirdventricular floor and at the region of the surgicalapproach, where the effect of the manipulation canbe directly inferred (Fig 3B and C).DiscussionThe adjustment of the brain parenchyma and theventricles to intracranial pressure conditions serves asone important morphologic indicator, in addition tothe clinical course of the patient, for success or failureof CSF draining surgery. It has been shown in severalstudies that these two criteria do not necessarily co-incide (5, 6, 8–10). In our opinion, the mere plani-metric assessment of the ventricular size is inappro-priate because it fails to reflect clinical improvementFIG 1. Sagittal view T2-weighted MRimage (8500/80 [TR/TE]; section thick-ness, 3 mm), obtained at 3 T on a BrukerMedspec 30/100 system in the midsag-ittal plane, suggests tri-ventricular hy-drocephalus due to aqueductal stenosis.A, Third ventricular floor vaults towardthe infundibular fossa.B, Postoperative condition 8 monthsafter surgery is shown.FIG 2. 3D rendering of the automatically segmented ventricular system during follow-up after endoscopic third ventriculostomy. Theunderlying 3D MR data sets were acquired preoperatively (T0) and postoperatively at 4 days (T1), 3 months (T2), and 8 months (T3) afterthe intervention. Measurement of the absolute ventricular volume yields 218, 177, 133, and 112 mL, respectively.378 PREUL AJNR: 25, March 2004due to subtle local changes. In this study, we presenta method to visualize and quantify the dynamics ofthe remodeling process.For the case presented herein, the pronouncedchanges in the surrounding of the third ventricle inthe early postoperative image reflect acute adjust-ments of the tissue to the altered pressure condition.In contrast, only minor changes can be observed inthe late postoperative images. We interpret this find-ing as chronic adaptations to the new balance of CSFcirculation. Our findings match those reported bySchwartz et al (9), who stated that direct measure-ment of intracranial pressure reveals a decrease witha delay of 4 to 8 days postoperatively. Moreover, theyhypothesized that ventricular volume might signifi-cantly decrease as early as the first 3 weeks aftersurgery. Our observations support this hypothesis inthat we were able to show a 19% reduction of theventricular volume as early as 4 days after surgery.During the next 3 months, the volume further de-creased by 20%. After 8 months, the ventricular vol-ume shrank another 10% (Fig 2). Accordingly, thethird ventricle shows massive early reconfiguration,whereas the subtle adaptations characterize the latercourse.We have shown that these adaptations can be ap-propriately visualized by means of displacement vec-tors. A quantification of the displacement vectors canbe enlisted as a criterion accompanying the clinicalcourse. This quantification can aid in comprehensionof the success or failure of the intervention. We applythis technique at our department on a routine basisfor all patients with hydrocephalus to assess postop-erative changes. In principle, such analysis is applica-ble for any disease for which careful observations ofsubtle tissue changes are particularly important.References1. Ernestus RI, Kru¨ger K, Ernst S, Lackner K, Klug N. Relevance ofmagnetic resonance imaging for ventricular endoscopy. Minim In-vasive Neurosurg 2002;45:72–772. Morota N, Watabe T, Inukai T, Hongo K, Nakagawa H. 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Schwartz TH, Ho B, Prestigiacomo CJ, Bruce JN, Feldstein NA,Goodman RR. Ventricular volume following third ventriculostomy.J Neurosurg 1999;91:20–2510. Schwartz TH, Yoon SS, Cutruzzola FW, Goodman RR. Thirdventriculostomy: post-operative ventricular size and outcome.Minim Invas Neurosurg 1996;39:122–12911. Buxton N, Turner B, Ramli N, Vloeberghs M. Changes in thirdventricular size with neuroendoscopic third ventriculostomy: ablinded study. J Neurol Neurosurg Psychiatry 2002;72:385–38712. Wolters, CH. Influence of tissue conductivity inhomogeneity andanisotropy to EEG/MEG based source localization in the humanbrain [PhD Thesis]. Leipzig: University of Leipzig; 200313. Hojjatoleslami SA, Kruggel F. Segmentation of large brain lesions.IEEE Trans Med Imaging 2001;20:666–66914. Schnack HG, Hulshoff HE, Baare WF, Viergever MA, Kahn RS.Automatic segmentation of the ventricular system from MR imagesof the human brain. Neuroimage 2001;14:95–10415. Tittgemeyer M, Wollny G, Kruggel F. Visualising deformationfields computed by non-linear image registration. Comput VisualSci 2002;5:45–5116. Wollny G, Kruggel F. Computational cost of non-rigid registrationalgorithms based on fluid dynamics. IEEE Trans Med Imaging2002;21:946–952AJNR: 25, March 2004 INTRACRANIAL PRESSURE RELIEF 379380 PREUL AJNR: 25, March 2004FIG 3. Shape difference of patient’s ventricular system. Colors indicate orientation and magnitude of shape difference; arrows indicatedisplacements.A, Preoperative versus early postoperative status.B, Superposition of displacement field, segmented ventricular system, and latest postoperative image obtained at the midsagittalplane.C, Detailed view into anatomy of third ventricle shows tissue adaptations to altered intracranial pressure condition.AJNR: 25, March 2004 INTRACRANIAL PRESSURE RELIEF 381

Quantitative assessment of parenchymal and ventricular readjustment to intracranial pressure relief

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