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Correlation of Diffusion Tensor Imaging Metrics with Neurocognitive Function in Chiari I Malformation Manoj Kumar1, Ram K. S. Rathore2, Arti Srivastava1, Santosh Kumar Yadav1, Sanjay Behari3, Rakesh Kumar Gupta1
Key words 䡲 Chiari I malformation 䡲 Corpus callosum 䡲 Diffusion tensor imaging 䡲 Fractional anisotropy 䡲 Mean diffusivity Abbreviations and Acronyms AD: Axial diffusivity CM: Chiari malformation CM-I: Chiari I malformation CM-II: Chiari II malformation DTI: Diffusion tensor imaging FA: Fractional anisotropy FCT A: Figure connection test MCP: Middle cerebellar peduncles MD: Mean diffusivity MRI: Magnetic resonance imaging NCT: Number connection tests NEX: Number of excitations NP: Neuropsychological PAT: Picture arrangement test RD: Radial diffusivity ROI: Region of interest SE: Spin echo TE: Echo time TR: Repetition time WAIS-P: Wechsler Adult Intelligence Scale-P WM: White matter From the Departments of 1Radiodiagnosis and 3 Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India; and 2 Departments of Mathematics and Statistics, Indian Institute of Technology, Kanpur, India. To whom correspondence should be addressed: Rakesh K. Gupta, M.D. [E-mail:
[email protected]]. Citation: World Neurosurg. (2011) 76, 1/2:189-194. DOI: 10.1016/j.wneu.2011.02.022 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter © 2011 Elsevier Inc. All rights reserved.
INTRODUCTION Chiari malformations (CMs) are structural defects in the brain. Normally the cerebellum and parts of the brain stem sit in an indented space at the lower rear of the skull, above the foramen magnum. When part of the cerebellum is located below the foramen magnum, it is called a CM (6). CMs typically fall within 1 of 4 categories (types I
䡲 BACKGROUND: The aim of this study was to examine changes in normalappearing deep gray and white matter regions of the brain in patients with Chiari I malformation compared with controls using diffusion tensor imaging (DTI) and to correlate these changes with neuropsychological (NP) test scores. 䡲 METHODS: Conventional magnetic resonance imaging, DTI, and neuropsychological tests were performed on 10 patients (median age 27 years, range 18 to 36 years) with Chiari I malformation and 10 age/sex-matched healthy controls. Diffusion tensor imaging metrics (fractional anisotropy, mean diffusivity [MD], radial diffusivity [RD], and axial diffusivity [AD]) were quantified in different regions of the brain in patients as well as in controls using the region of interest (ROI) method. An independent Student t test was performed to evaluate differences in diffusion tensor imaging metrics from patients and controls. Pearson’s correlation coefficient was also used to determine association between NP test scores and DTI metrics in patients. 䡲 RESULTS: Significantly reduced fractional anisotropy with increased MD was found in genu, splenium, fornix, and putamen in patients compared with controls; however, RD significantly increased in fornix and cingulum, whereas AD significantly increased in putamen, thalamus, and fornix as compared with controls. NP tests were found to be abnormal in patients with Chiari I malformation compared with controls, and some of these tests showed significant correlation with DTI metrics. 䡲 CONCLUSIONS: We conclude that abnormal changes in the DTI metrics in patients with Chiari I malformation indicate microstructural abnormalities in different brain regions that may be associated with neurocognitive abnormalities.
to IV) depending on the degree of displacement as well as the varying etiology of the malformation (6). Chiari I malformation (CM-I) is defined radiographically as a simple displacement of the cerebellar tonsils 5 mm or more below the foramen magnum (9). Displacements of the cerebellar tonsils result in pressure on the cerebellum and brainstem that may affect functions controlled by these areas and block the flow of cerebrospinal fluid. The cerebellum controls motor activity, coordination, and fine motor function and also plays a role in cognitive function in terms of attention and language (9, 22). Patients with CM-I frequently complain of headache, dizziness, disequilibrium, tinnitus, difficulty in swal-
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lowing, palpitation, sleep apnea, muscle weakness, chronic fatigue, and painful tingling of the hands and feet (4, 16). Determination of prevalence is difficult because many children born with CM-I may be asymptomatic until adolescence or adulthood; the malformation may be discovered incidentally during the diagnosis and treatment of another complaint (5). Diffusion tensor imaging (DTI) has provided quantitative assessment of water diffusion in tissues by quantifying isotropic and anisotropic diffusion (18). Commonly used DTI metrics are mean diffusivity (MD), which measures the magnitude of diffusion, and fractional anisotropy (FA), which quantifies preferential direction of water diffusion along white matter
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Figure 1. Midsagittal T1-weighted image (A) demonstrates protrusion of the cerebellar tonsils (arrow) below the foramen magnum in a 25-year-old female patient with Chiari I malformation. The brainstem and cerebellar hemispheres appear normal. The axial (B-D) and sagittal (E) color-coded FA maps at the level of the third ventricle, corona radiata, pons and massa intermedia showing placement of region of interest on caudate nuclei,
(WM) tracts. DTI along with cognitive measures have been shown to be useful in elucidating the relationship between integrity of WM pathways and efficiency of cognitive and neural processing during normal brain development (19). A previous DTI study has reported abnormal FA in commissural pathways in patients with Chiari II malformation (CM-II) with neuropsychological deficits (14). However, there is no study describing WM changes in the brain in CM-I patients using DTI and its correlation with neuropsychological (NP) tests. We hypothesized that the neurocognitive abnormalities in these patients may be associated with changes in deep gray and WM microstructure. The aim of this study was to compare the changes in DTI metrics quantified from normal-appearing deep gray and WM regions of the brain in patients
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thalamus, and putamen, Cingulum, middle cerebellar peduncles, genu, and splenium of corpus callosum and fornix, respectively. The threshold value of the color-coded FA map for display is kept at 0.2, above which the color-coded regions reflect the white matter only (red [right-left], green [anterior-posterior] and blue [superior-inferior]). FA ⫽ fractional anisotropy.
and controls. We also looked for correlation, if any, in DTI metrics in various brain regions with NP test scores.
MATERIALS AND METHODS The present study was performed on 10 patients with CM-I (7 male and 3 female patients, ages 18 to 36 years) and 10 age/sexmatched controls (8 male and 2 female patients, ages 18 to 32 years). All subjects included in this study were right handed. These patients presented with headache and dizziness and were sent for routine magnetic resonance imaging (MRI) evaluation and were included in the study when the ventricles were normal on imaging. Informed consent was obtained from each
subject to perform the study. The study was performed within the guidelines of the institutional ethics committee.
Diagnosis of CM-I CM-I was diagnosed on the basis of displacement of the cerebellar tonsils 5 mm or more below the foramen magnum (9).
Conventional MRI Protocol Imaging was performed on 1.5-T GE MRI scanner (General Electric Medical System, Milwaukee, Wisconsin, USA) using a standard quadrature birdcage receive-andtransmit radiofrequency head coil. Conventional MRI protocol included T2-weighted fast spin echo images with repetition time
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Table 1. Comparison of Fractional Anisotropy and Mean Diffusivity (⫻ 10⫺3 mm2/s) Values in Deep Gray and White Matter Using Region-of-Interest Analysis Between Controls and Chiari I Malformation Patients Mean Diffusivity (ⴛ 10ⴚ3 mm2/s)
Fractional Anisotropy Control
CM-I
P value
Control
CM-I
P value
Caudate nuclei
0.20 ⫾ 0.01
0.19 ⫾ 0.01
0.23
0.74 ⫾ 0.02
0.75 ⫾ 0.02
0.06
Putamen
0.18 ⫾ 0.02
0.15 ⫾ 0.02
0.04
0.70 ⫾ 0.03
0.73 ⫾ 0.04
0.05
Thalamus
0.30 ⫾ 0.01
0.29 ⫾ 0.01
0.27
0.72 ⫾ 0.03
0.75 ⫾ 0.03
0.07
Genu
0.55 ⫾ 0.04
0.50 ⫾ 0.030
0.01
0.77 ⫾ 0.06
0.83 ⫾ 0.05
0.02
Splenium
0.57 ⫾ 0.07
0.51 ⫾ 0.04
0.04
0.74 ⫾ 0.04
0.83 ⫾ 0.08
0.01
Fornix
0.41 ⫾ 0.07
0.34 ⫾ 0.05
0.03
0.90 ⫾ 0.08
0.98 ⫾ 0.01
0.01
Cingulum
0.42 ⫾ 0.06
0.38 ⫾ 0.06
0.17
0.72 ⫾ 0.04
0.77 ⫾ 0.02
0.01
MCP
0.62 ⫾ 0.07
0.60 ⫾ 0.08
0.54
0.66 ⫾ 0.15
0.64 ⫾ 0.12
0.30
Regions
CM-I, Chiari I malformation; FA, fractional anisotropy; MCP, middle cerebellar peduncle; MD, mean diffusivity.
(TR) (ms)/echo time (TE)(ms)/number of excitations (NEX) ⫽ 6000/85/4 and spin echo (SE) T1-weighted images with TR/ TE/NEX ⫽ 1000/14/2. Both T1- and T2weighted axial images were acquired using 3-mm slice thickness, no interslice gap, 240 ⫻ 240 mm2 field of view and 256 ⫻ 256 image matrix.
DTI Protocol DTI data were acquired using a single-shot echo-planar dual SE sequence with ramp sampling (15). Diffusion-weighted acquisition parameters were: b-factor ⫽ 0 and 1000 s/mm2, slice thickness ⫽ 3 mm without interslice space, number of slices ⫽ 34 to 38, field of view ⫽ 240 ⫻ 240 mm2, TR ⫽ 8 seconds, TE ⫽ 100 ms, NEX ⫽ 8, and image matrix of 256 ⫻ 256 (following zero-filling). The diffusion tensor encoding used was the balanced rotationally invariant scheme (3) with 10 uniformly distributed directions over the unit hemisphere. The DTI imaging was completed in 9 minutes and 36 seconds. DTI data were processed and evaluated using a Java-based program as described elsewhere (20). Regions of interest (ROIs) analysis was performed for the quantification of DTI metrics in different regions of the brain in patients and controls.
ROI Analysis DTI-derived maps were displayed and overlaid on images with T2 contrast to facilitate ROI placement in both white and gray mat-
ter regions. Elliptical/rectangular ROIs varying from 2 ⫻ 2 and 6 ⫻ 6 pixels were placed in different brain regions including basal ganglia (caudate nuclei, thalamus, and putamen at the level of third ventricle) and WM (cingulum at the level of corona radiata; fornix, genu, and splenium at the level of massa intermedia and middle cerebellar peduncles (MCP), in both controls and patients (Figure 1). NP Tests NP tests were performed on patients and controls. NP tests included trial making test (number connection tests [NCT A, B] and figure connection test [FCT A]) as well as the performance subset of modified Wechsler Adult Intelligence Scale [WAIS-P, modified for Indian population], which included the picture completion test, digit symbol test, picture arrangement test [PAT], object assembly test, and block design test. These tests have been used in other studies of similar pathologies, such as CM-II and other cerebellar disorders (24, 26, 27). In NCT and FCT A, lower scores represent better performance, whereas in WAIS-P, a higher score represents better performance. The trial making test assesses visual motor coordination, concentration, mental speed, memory alteration, and attention; however, WAIS-P tests evaluate visuospatial capacity and visuomotor speed. Statistical Analysis Bivariate analysis of correlation was performed to rate interrater reliability between
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2 observers, with the assumption that there was no correlation between DTI measures and NP test scores (Ho [null hypothesis] ⫽ 0). Alternatively, if a correlation of more than 0.001 was observed at ␣ ⫽ 0.05% and 90% power of test, the null hypothesis was rejected. We performed paired sample Student t test between left and right measurement of FA, MD, axial diffusivity (AD), and radial diffusivity (RD) values in controls and patients and did not find any statistically significant difference. Therefore, FA, MD, RD, and AD values from left and right measurements in all regions were pooled together in both patients and controls for the final data set for statistical analysis. An independent Student t test was performed to evaluate differences in DTI-derived metrics in patients and controls. Pearson’s correlation coefficients were computed to determine association between NP test scores and DTI metrics. A P value ⱕ0.05 was considered to be statistically significant. All statistical data computations were performed using Statistical Package for Social Sciences (SPSS, version 16.0 SPSS, Inc, Chicago, Illinois, USA).
RESULTS On conventional MRI, no abnormality was seen in any region of the brain except cerebellar tonsillar herniation more than 5 mm below the foramen magnum, ie, a characteristic feature of CM-I. None of these patients had hydrocephalus brain.
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Table 2. Comparison of Axial Diffusivity (⫻ 10⫺3 mm2/s) and Radial Diffusivity (⫻ 10⫺3 mm2/s) Values in Deep Gray and White Matter Between Controls and Chiari I Malformation Patients AD (ⴛ 10ⴚ3 mm2/s)
RD (ⴛ 10ⴚ3 mm2/s)
Control
CM I
P value
Control
CM I
P value
Caudate nucleus
0.81 ⫾ 0.02
0.83 ⫾ 0.75
0.211
0.48 ⫾ 0.01
0.50 ⫾ 0.02
0.121
Putamen
0.75 ⫾ 0.03
0.80 ⫾ 0.04
0.009
0.47 ⫾ 0.02
0.49 ⫾ 0.02
0.089
Thalamus
0.82 ⫾ 0.02
0.85 ⫾ 0.03
0.034
0.47 ⫾ 0.02
0.49 ⫾ 0.01
0.085
Genu
1.29 ⫾ 0.15
1.33 ⫾ 0.09
0.589
0.38 ⫾ 0.04
0.38 ⫾ 0.05
0.842
Splenium
1.34 ⫾ 0.10
1.39 ⫾ 0.06
0.265
0.34 ⫾ 0.05
0.37 ⫾ 0.06
0.153
Fornix
1.46 ⫾ 0.18
1.73 ⫾ 0.17
0.003
0.51 ⫾ 0.06
0.70 ⫾ 0.11
0.001
Cingulum
1.08 ⫾ 0.06
1.11 ⫾ 0.06
0.384
0.37 ⫾ 0.03
0.42 ⫾ 0.03
0.016
MCP
0.74 ⫾ 0.43
0.87 ⫾ 0.13
0.398
0.18 ⫾ 0.12
0.22 ⫾ 0.08
0.375
Regions
P ⬍ 0.05 was considered statistically significant. AD, axial diffusivity; CM-I, Chiari I malformation; MCP, middle cerebellar peduncle; RD, radial diffusivity.
Quantitative Analysis Interrater and intrarater reliability values for the ROI analysis-based approach were 0.85 and 0.92 (P ⬍ 0.01), respectively. The mean FA, MD, AD, and RD values obtained from different regions of the brain in patients and controls are summarized in Tables 1 and 2. FA, MD, AD, and RD Values from Deep Gray and WM Regions in Patients with CM-I In putamen, significantly decreased FA along with increased MD was observed in
patients compared with controls. However, no significant changes in FA and MD values were found in caudate nuclei and thalamus in patients as compared with controls. We observed a significant decrease in FA along with increased MD in genu, splenium, and fornix in patients as compared with controls. No statistical significance was observed in FA in cingulum and MCP in patients compared with controls. Significantly increased MD was observed in cingulum; however, in MCP the MD was not statically significant in patients compared with controls (Table 1). AD of putamen, thalamus, and fornix
Figure 2. Bar diagram showing scores of various neuropsychological tests in healthy controls and patients with Chiari malformation I. Trial-making tests include number connection tests (NCT A, B) and figure connection test (FCT A), and the Wechsler Adult Intelligence Scale-P test included the picture connection test (PCT), digit symbol test (DST), block design test (BDT), picture arrangement test (PAT), and 5-object assembly test (OAT). *Significant difference in NPT scores (P ⬍ 0.05) between controls and patients with Chiari malformation I.
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showed a significant increase compared with controls; however, it did not reach at the level of significance in caudate nucleus, genu, splenium, cingulum, and MCP (Table 2). RD of fornix and cingulum showed a significant increase as compared with controls; however, it did not reach the significant level in caudate nucleus, putamen, thalamus, genu, splenium, and MCP (Table 2).
Neuropsychological Test NCT A and B and FCT A scores were significantly higher, whereas picture completion test, object assembly test, PAT, block design test, and digit symbol test scores were significantly lower in patients with CM-I as compared with controls (Figure 2).
Correlation Between DTI Metrics and NP Test Scores in Patients with CM-I A significant inverse correlation was found between NCT A and FA in genu (r ⫽ ⫺0.74, P ⫽ 0.01) and splenium (r ⫽ ⫺0.80, P ⫽ 0.01), respectively. We observed a positive correlation between FA and PAT in genu (r ⫽ 0.70, P ⫽ 0.03). FA showed a significant inverse correlation with NCT B in cingulum (r ⫽ ⫺0.76, P ⫽ 0.01) and fornix (r ⫽ ⫺0.72, P ⫽ 0.02), respectively. A significant positive correlation was observed between MD and NCT A in MCP (r ⫽ 0.61, P ⫽ 0.04) and PAT in cingulum (r ⫽ 0.82, P ⫽ 0.01), respectively. AD values did not show any significant correlation with NP test scores in any re-
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gions. RD values of genu positively correlate with FCT A (r ⫽ 0.692, P ⫽ 0.027), whereas those from thalamus negatively correlate with PC (r ⫽ ⫺0.697, P ⫽ 0.025), MCP with BD (r ⫽ ⫺670, P ⫽ 0.034) and cingulum with PA (r ⫽ ⫺0.637, P ⫽ 0.048).
DISCUSSION The current study demonstrates significantly decreased FA along with increased MD value in genu, splenium, fornix, and putamen as compared with controls; however, AD significantly increased in putamen, thalamus, and fornix, whereas RD significantly increased in fornix and cingulum as compared with controls. These patients also showed abnormal NP test scores as compared with controls, and some of these test scores showed significant correlation with DTI indices in different regions of the brain. Previous studies have reported reduced FA in corpus callosum and explained on the basis of WM damage due to increased cerebrospinal fluid (CSF) pressure secondary to acute hydrocephalous in patients with CM-II having meningomyelocele (14). In the current study, all patients were without hydrocephalous, thus the reason for increased pressure that causes reduction in FA in these patients is unclear. Herweh et al. (14) have reported a lower FA in corpus callosum in patients with Chiari II malformation even in the absence of hydrocephalous. In the current study, injury to the corpus callosum during development (10) and/or neuronal degeneration (1) may be responsible for reduced FA along with increased MD in genu and splenium. The caudate nuclei plays a critical role in supporting the planning and execution of strategies and behavior required for achieving goal-oriented actions. This is in contrast to putamen, which appears to provide cognitive functions more limited to stimulus-response. Increased FA has been reported in basal ganglia in patients with spina bifida and Huntington disease (7, 13). Barnea-Goraly et al. (2) have reported reduced anisotropy with increased caudate volume in children with fragile X syndrome and explained on the basis of excessive growth and disorganized arborization of dendrites. Targeted dendrite elimination in caudate nuclei has been reported in various neurodegenerative disorders (7, 29). In our study, we
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found significantly decreased FA along with increased MD in putamen, and speculate that it might be due to elimination of dendrite arborization. Eigen values can serve as markers of axon and myelin integrity (28). The exact neurobiological principles governing AD and RD are unknown, but AD is sensitive to axonal integrity, and a lower value can be caused by axonal pruning, cytoskeleton formation during axonal development, or Wallerian degeneration (11, 12, 28). In contrast, RD is sensitive to myelin integrity, and a higher value may result from dysmyelination or demyelination (25). In the present study, we also observed significantly increased RD values in fornix and cingulum compared with controls. We speculate that patients with CM-1 probably have abnormal myelin integrity, which may also contribute to the abnormal cognitive function in these patients. Limited studies have been reported on cerebellar WM maturation in normal children (8, 23); however, abnormal maturational studies in MCP have not been reported so far. A recent DTI study has demonstrated increased FA along with decreased MD in MCP in normal children as they grow up from birth to 11 years (23). In the current study, reduced MD values were observed in MCP in patients with CM-I compared with controls. These abnormal DTI indices may due to abnormal cerebellar WM development in these patients. The neuropsychological measures have been used to assess the areas of cognitive functioning found to be impaired in patients with CM- II. There is some evidence that individual differences in microstructural integrity account for variation in a wide range of neurocognitive functions. There are only a few studies reported describing the relationship between anomalies in various brain regions seen on DTI and neurocognitive functions in patients with CM-II (14, 26); however; no study is available in patients with CM-I. To the best of our knowledge, this is the first study that describes neuropsychological abnormalities in CM-I and its correlation with DTI metrics. Generally, patients with CM experience problems with memory alteration and visuospatial orientation, motor speed, concentration, and attention deficits (14). In patients with
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myelomeningocele and CM-II, abnormalities in the limbic system have been shown to be correlated with emotion, memory, and learning complexities (26). In this study, patients showed significantly poor performance in all components of NP test scores as compared with controls, suggesting that these patients have cognitive defects similar to what has been reported in CM-II. In this study, we observed a significant inverse correlation between DTI indices in genu and splenium with NCT A and NCT B. It has been reported that NCT A and NCT B reflect the executive functioning, mental attention, and visuospatial skills (24). For these skills, transhemispheric integration between primary and supplementary visual areas of both hemisphere is required (17). Previous studies have reported association between low callosal FA and neurocognitive deficits (14, 21). In this study, decreased callosal FA inversely correlated with NCT A and NCT B, which is consistent with a recent study in patients with CM-II associated with reduced visuospatial skills (14). A significant positive correlation between FA and PAT in genu may indicate deficits in logical and sequential reasoning in these patients. The presence of a significant correlation of RD with FCT A, PC, BD, and PA in genu, thalamus, MCP, and cingulum, respectively, suggests that these changes may be associated with neurocognitive functions in these patients. However, a small sample size and the use of the ROI approach to quantifying the DTI metrics may be considered limitations of the study.
CONCLUSIONS In conclusion, our study demonstrates abnormal changes in the magnitude and anisotropy of water diffusion in patients with CM-I, which indicates microstructural abnormalities in the different brain regions/ tracts using DTI, even when they appear normal on conventional MRI. Correlation of some of these abnormal NP tests with DTI-derived metrics suggests that the microstructural abnormalities may form the basis for neurocognitive deficits in these patients. Because these patients were found to have neuropsychological abnormalities along with DTI metrics changes, they may be evaluated in the future to see the effect of surgical decompression on the NP test
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scores as well as the DTI metrics in the future.
REFERENCES 1. Assaf Y, Ben-sira L, Constantini S, Chang LC, Beniadani L: Diffusion tensor imaging in hydrocephalus: initial experience. Am J Neuroradiol 27:1717-1724, 2006. 2. Barnea-Goraly N, Eliez S, Hedeus M, Menon V, White CD, Moseley M, Reiss AL: White matter tract alterations in fragile X syndrome: preliminary evidence from diffusion tensor imaging. Am J Med Genet B Neuropsychiatr Genet 118:81-88, 2003. 3. Batchelor PG, Atkinson D, Hill D, Calamante F, Connelly A: Anisotropic noise propagation in diffusion tensor MRI sampling schemes. Magn Reson Med 49:1143-1151, 2003. 4. Caetano de Barros M, Azevedo Filho HC, Spinelli C: Disturbances of sexual potency in patients with basilar impression and Arnold-Chiari malformation. J Neurol Neurosurg Psychiatry 38:598-600, 1975. 5. Caldwell DL, Dubose CO, White TB: Chiari Malformations: Radiol Technol 80:340-354, 2009. 6. Chiari H: Uber Veranderungen des Kleinhirns in folge von Hydrocephalie des Grosshirns. Dtsch Med Wochenschr 17:1172-11725, 1891. 7. Douaud G, Gaura V, Ribeiro MJ, Lethimonnier F, Maroy R, Verny C, Krystkowiak P, Damier P, Bachoud-Levi AC, Hantraye P, Remy P: Distribution of grey matter atrophy in Huntington’s disease patients: a combined ROI-based and voxel-based morphometric study. Neuroimage 32:1562-1575, 2006. 8. Dubois J, Hertz-Pannier L, Dehaene-Lambertz G, Cointepas Y, Le-Bihan D: Assessment of the early organization and maturation of infants’ cerebral white matter fiber bundles: a feasibility study using quantitative diffusion tensor imaging and tractography. Neuroimage 30:1121-1132, 2006. 9. Elster AD, Chen MY: Chiari I malformations: clinical and radiologic reappraisal. Radiology 183:347353, 1992. 10. Ewing-Cobbs L, Barnes MA, Fletcher JM: Early brain injury in children: development and reorganization
194
www.SCIENCEDIRECT.com
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of cognitive function. Dev Neuropsychol 24:669704, 2003. 11. Gao W, Lin W, Chen Y, Gerig G, Smith JK, Jewells V, Gilmore JH: Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. AJNR Am J Neuroradiol 30: 290-296, 2009. 12. Gross DW, Bastos A, Beaulieu C: Diffusion tensor imaging abnormalities in focal cortical dysplasia. Can J Neurol Sci 32:477-482, 2005. 13. Hasan KM, Sankar A, Halphen C, Kramer LA, Ewing-Cobbs L: Quantitative diffusion tensor imaging and intellectual outcomes in spina bifida: laboratory investigation. J Neurosurg Pedia 2:75-82, 2008.
of diffusion tensor imaging parameters in white matter tracts of preterm newborns. J Magn Reson Imaging 22:467-474, 2005. 22. Rapoport M, van Reekum R, Mayberg H: The Role of the Cerebellum in Cognition and Behavior: A Selective Review. J Neuropsychiatry Clin Neurosci 12:2, 2000. 23. Saksena S, Husain N, Malik GK, Trivedi R, Sarma M, Rathore RS, Pandey CM, Gupta RK: Comparative evaluation of the cerebral and cerebellar white matter development in pediatric age group using quantitative diffusion tensor imaging. Cerebellum 7:392-400, 2008. 24. Schmahmann JD, Sherman JC: The cerebellar cognitive affective syndrome. Brain 121:561-579, 1998.
14. Herweh C, Akbar M, Wengenroth M, Blatow M, Mair-Walther J, Rehbein N, Nennig E, Schenk JP, Heiland S, Stippich C: DTI of Commisural fibers in patients with Chiari-malformation. Neuroimage 44: 306-311, 2009.
25. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC: Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26:132-140, 2005.
15. Le Bihan D: Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci 4:469-480, 2003.
26. Vachha B, Adams RC, Rollins NK: Limbic tract anomalies in pediatric myelomeningocele and Chiari II malformation: anatomic correlations with memory and learning-initial investigation. Radiology 240: 194-202, 2006.
16. Martins HA, Ribas VR, Lima MD, Oliveira DA, Viana MT, Ribas KH, Valença MM: Headache precipitated by Valsalva maneuvers in patients with congenital Chiari I malformation. Arq Neuropsiquiatr 68:406409, 2010. 17. McLaughlin NC, Paul RH, Grieve SM, Williams LM, Laidlaw D, DiCarlo M, Clark CR, Whelihan W, Cohen RA, Whitford TJ, Gordon E: Diffusion tensor imaging of the corpus callosum: a cross-sectional study across the lifespan. Int J Dev Neuroscience 25:215-221, 2007. 18. Mori S, Zhang J: Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527-539, 2006.
27. Vinck A, Maassen B, Mullaart R, Rotteveel J: ArnoldChiari-II malformation and cognitive functioning in spina bifida. J Neurol Neurosurg Psychiatry 77: 1083-1086, 2006. 28. Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S: Fiber tract-based atlas of human white matter anatomy. Radiology 230:77-87, 2004. 29. Zaja-Milatovic S, Milatovic D, Schantz AM, Zhang J, Montine KS, Samii A, Deutch AY, Montine TJ: Dendritic degeneration in neostriatal medium spiny neurons in Parkinson disease. Neurology 64: 545-547, 2005.
19. Munakata Y, Casey BJ, Diamond A: Developmental cognitive neuroscience: progress and potential. Trends Cogn Sci 3:122-128, 2004.
Conflict of interest statement: Manoj Kumar and Santosh K. Yadav acknowledge the financial assistance from the Indian Council of Medical Research (ICMR), New Delhi, India.
20. Nath K, Saraswat VA, Krishna YR, Thomas MA, Rathore RK, Pandey CM, Gupta RK: Quantification of cerebral edema on diffusion tensor imaging in acute-on-chronic liver failure. NMR Biomed 2:713722, 2008.
received 14 August 2010; accepted 5 February 2011
21. Partridge SC, Mukherjee P, Berman JI, Henry RG, Miller SP, Lu Y, Glenn OA, Ferriero DM, Barkovich AJ, Vigneron DB: Tractography-based quantitation
Citation: World Neurosurg. (2011) 76, 1/2:189-194. DOI: 10.1016/j.wneu.2011.02.022 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter © 2011 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, DOI:10.1016/j.wneu.2011.02.022
