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Diffusion Tensor Imaging Demonstrates Brainstem and Cerebellar Abnormalities in Congenital Central Hypoventilation Syndrome

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Diffusion Tensor Imaging Demonstrates Brainstem and Cerebellar Abnormalities in Congenital Central Hypoventilation Syndrome 0031-3998/08/6403-0275 Vol. 64, No. 3, 2008 PEDIATRIC RESEARCH Printed in U.S.A. Copyright © 2008 International Pediatric Research Foundation, Inc. Diffusion Tensor Imaging Demonstrates Brainstem and Cerebellar Abnormalities in Congenital Central Hypoventilation Syndrome RAJESH KUMAR, PAUL M. MACEY, MARY A. WOO, JEFFRY R. ALGER, AND RONALD M. HARPER Department of Neurobiology [R.K., R.M.H.], Department of Neurology [J.R.A.], Brain Research Institute [P.M.M., R.M.H.], School of Nursing [P.M.M., M.A.W.], University of California at Los Angeles, Los Angeles, California 90095 ABSTRACT: Congenital central hypoventilation syndrome (CCHS) the initial developmental injury in CCHS (6), primarily target patients show reduced breathing drive during sleep, decreased hy- autonomic ganglia, which lie in peripheral and brainstem sites, poxic and hypercapnic ventilatory responses, and autonomic and and may result in cellular and axonal deficits. However, affective deficits, suggesting both brainstem and forebrain injuries. previously used MRI procedures, which demonstrate injury to Forebrain damage was previously described in CCHS, but method- rostral brain areas, show little evidence of expected brainstem ological limitations precluded detection of brainstem injury, a con- injury. Technical limitations associated with spatial resolution cern because genetic mutations in CCHS target brainstem autonomic and sensitivity have precluded detection of brainstem injury. nuclei. To assess brainstem and cerebellar areas, we used diffusion tensor imaging-based measures, namely axial diffusivity, reflecting Thus, injury to much of the reflex circuitry for breathing and water diffusion parallel to fibers, and sensitive to axonal injury, and parasympathetic motor neuron action that lies in brainstem and radial diffusivity, measuring diffusion perpendicular to fibers, and cerebellar sites (7,8) have not been adequately assessed. These indicative of myelin injury. Diffusion tensor imaging was performed regions do, however, show functional MR deficits to ventilatory in 12 CCHS and 26 controls, and axial and radial diffusivity maps and cold pressor challenges in CCHS subjects (9–11). were compared between groups using analysis of covariance (covari- Among MRI techniques, DTI is a procedure that measures ates; age and gender). Increased axial diffusivity in CCHS appeared directional diffusivity of water molecules. Although several within the lateral medulla and clusters with injury extended from the DTI-based indices, including mean-diffusivity, can detect dorsal midbrain through the periaqueductal gray, raphe´, and superior brain tissue injury, and show rostral brain damage and some cerebellar decussation, ventrally to the basal-pons. Cerebellar cortex degree of brainstem injury in CCHS (4), these indices are not and deep nuclei, and the superior and inferior cerebellar peduncles specific to different types of underlying pathology, and may be showed increased radial diffusivity. Midbrain, pontine, and lateral insufficiently sensitive to reveal subtle tissue changes. Spe- medullary structures, and the cerebellum and its fiber systems are injured in CCHS, likely contributing to the characteristics found in cialized DTI indices, such as axial diffusivity, a measure of the syndrome. (Pediatr Res 64: 275–280, 2008) diffusivity parallel to axons, and radial diffusivity, a measure of diffusivity perpendicular to fibers (12), provide markedly enhanced sensitivity to tissue injury. Animal studies infer that ongenital central hypoventilation syndrome (CCHS) is a axial diffusivity abnormalities accompany axonal injury, while C developmental condition characterized by a loss of the radial diffusivity changes appear with altered myelin (12–14), drive to breathe during sleep, reduced ventilatory sensitivity to and both measures are more sensitive compared with other CO2 and O2, and multiple thermoregulatory, affective, and DTI-based indices. autonomic deficiencies (1–3). The affective and thermoregu- The objective was to evaluate, using axial and radial diffu- latory functions depend on more-rostral brain sites, such as the sivity measures, the extent of injury in brainstem and cerebel- hypothalamus and limbic regions, and these areas show injury lar sites in CCHS, and determine whether damage occurs in with quantitative magnetic resonance imaging techniques, sites contributing to syndrome characteristics. such as T2 relaxometry and diffusion tensor imaging (DTI)- based mean diffusivity measures (4,5). METHODS Although several physiologic and emotional deficits in CCHS result from rostral brain injury, other breathing and Subjects. We studied 12 CCHS subjects (mean age Ϯ SD: 15.2 Ϯ 2.4 y; range: 12–18 y; 8 male) and 26 control subjects (15.5 Ϯ 2.4 y; 10–19 y; 15 autonomic problems, such as diminished ventilatory sensitiv- male). CCHS subjects were diagnosed based on standard criteria (3), and ity to CO2 and parasympathetic deficits implicate brainstem recruited through the CCHS family network (http://www.cchsnetwork.org). involvement. Mutations of PHOX2B, suggested to underlie Of 12 CCHS subjects, four showed evidence of PHOX2B mutation, two were inconclusive, and six subjects were never tested. Some CCHS patients require continuous ventilatory support during sleep and waking; we included only cases requiring breathing assistance during sleep. CCHS subjects with addi- Received January 2, 2008; accepted April 23, 2008. tional conditions, such as cardiovascular or neurologic disorders, which can Correspondence: Ronald M. Harper, Ph.D., Department of Neurobiology, David Geffen School of Medicine at UCLA, University of California at Los Angeles, Los Angeles, CA 90095-1763; e-mail: [email protected] Supported by the National Institute of Child Health and Human Development R01 Abbreviations: CCHS, Congenital central hypoventilation syndrome; DTI, HD-22695. Diffusion tensor imaging; NTS, Nucleus of the solitary tract 275 276 KUMAR ET AL. also affect brain tissue structure (e.g., loss of hippocampal tissue in temporal Region-of-interest analyses. Regions-of-interest were created for clusters lobe epilepsy), were excluded. CCHS subjects with Hirschsprung’s disease showing increased axial diffusivity only, radial diffusivity alone, and both were also excluded to avoid concomitant neural injury from intestinal mal- increased axial and radial diffusivity in brainstem and cerebellar regions, absorption, e.g., thiamine deficiency. Control subjects were recruited through based on voxel-based-analyses procedures for all distinct locations. Using advertisements at the university campus, which has a diverse ethnic popula- these region-of-interest masks, mean axial and radial diffusivity values were tion; the aim was to target parents who could enroll their children. All studies derived from each individual’s normalized and smoothed axial and radial were performed without anesthesia or sedatives; subjects were conscious diffusivity maps, and significant group differences for these distinct brain throughout, and were given breaks from the scanner if they became restless. locations were evaluated using multivariate analysis of covariance (SPSS, All subjects and their parents/guardians provided informed written con- v15, Chicago, IL), with age and gender included as covariates. sent/assent, and the procedures were approved by the Institutional Review Comparison of structural injury and earlier-described functional ϩ Board of the University of California at Los Angeles. deficits. We had earlier performed hypercapnic (5%CO2 95%O2), hypoxic ϩ Magnetic resonance imaging. Brain MRI studies were performed using a (15%O2 85%N2), and cold pressor (forehead) challenges in CCHS children 3.0-Tesla MRI scanner (Magnetom Trio; Siemens, Erlangen, Germany), with during functional MRI (9–11). Thirteen to 14 CCHS and 14 control subjects a whole-body transmitter coil, and a receive-only 8-channel phased-array were examined with a conventional blood-oxygen-level-dependent MRI pro- head-coil. Foam pads were placed on both sides of the head to minimize head tocol; a baseline series was collected, followed by challenges (hypercapnia, motion. High-resolution T1-weighted imaging was performed using a mag- hypoxia, and cold pressor) with 10 min rest intervals. The functional series netization-prepared-rapid-acquisition-gradient-echo pulse sequence [repeti- were evaluated with cluster and volume-of-interest analyses (9–11). Clusters tion-time (TR) ϭ 2200 ms; echo-time (TE) ϭ 3.05 ms; inversion-time ϭ 1100 showing functional deficits between groups were compared with structural ms; flip-angle ϭ 10°; matrix size ϭ 256 ϫ 256; field-of-view (FOV) ϭ 220 ϫ injuries found here. 220 mm; slice thickness ϭ 1.0 mm]. Proton-density (PD) and T2-weighted images were collected, using a dual-echo turbo spin-echo pulse sequence (TR ϭ 8000 ms; TE1, 2 ϭ 17, 133 ms; flip-angle ϭ 150°; matrix size ϭ RESULTS 256 ϫ 256; FOV ϭ 240 ϫ 240 mm; slice thickness ϭ 5.0 mm; turbo factor ϭ 5). DTI was performed in the axial plane, using a single-shot Visual examination of T1-, T2-, and PD-weighted images spin-echo echo-planar pulse sequence (TR ϭ 10,000 ms; TE ϭ 87 ms; from CCHS subjects showed no obvious abnormalities in flip-angle ϭ 90°; matrix size ϭ 128 ϫ 128; FOV ϭ 220 ϫ 220 mm; thickness ϭ 1.9 mm; slices ϭ 75; no interslice gap; diffusion gradient brainstem and cerebellar regions. However, axial and radial directions ϭ 12; b ϭ 0, 50, 700 s/mm2). The parallel imaging technique, diffusivity measures showed multiple brainstem and cerebellar generalized-autocalibrating-partially-parallel-acquisition
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