Neuroscience Letters 557 (2013) 79–83

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CST recovery in pediatric hemiplegic patients: Diffusion tensor tractography study Seung Ok Baek a , Sung Ho Jang a , Eusil Lee b , Saeyoon Kim b , Jeong Ok Hah b , Yong Hoon Park b , Jae Min Lee b , Su Min Son a,∗ a b

Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, Republic of Korea Department of Pediatrics, College of Medicine, Yeungnam University, Republic of Korea

h i g h l i g h t s • • • • •

Investigation of CST recovery in 29 hemiplegic patients. More increase of FA value of more affected CST than FA of less affected CST at FU DTI. Decrease of asymmetric anisotropy (AA) between both CST at FU DTI. Significant correlation of AA change with FA change of more affected CST. No significant correlation of AA change with FA change of less affected CST.

a r t i c l e

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Article history: Received 1 July 2013 Received in revised form 3 October 2013 Accepted 21 October 2013 Keywords: Diffusion tensor Corticospinal tract Motor Hemiplegia Cerebral palsy

a b s t r a c t Many diffusion tensor imaging (DTI) studies have reported an association between corticospinal tract (CST) injury and motor dysfunction. In this study, we investigated CST recovery in 29 pediatric patients with clinical hemiplegia using DTI. We measured the fractional anisotropy (FA), apparent diffusion coefficient (ADC), and asymmetric anisotropy (AA) of both CSTs. The patients were classified into three groups according to severity of CST disruption of the more affected hemisphere. DTI was followed up for 9.34 ± 2.07 months after initial evaluation. The FA value of the more affected CST showed a significant decrease compared to the opposite side at initial and follow up evaluation, respectively (p < 0.05). The FA value of both CSTs showed a significant increase at follow up compared to the initial evaluation, while more changes were observed on the more affected side, compared with the less affected side (p < 0.05). AA showed a significant decrease at follow up, and showed significant correlation with interval change of FA value of the more affected side, not with that of the less affected side (r = 0.543, p < 0.05). 19 patients showed change of CST integrity. In the current study, the results of DTI showed recovery of the CST and provided radiologic evidence for a scientific basis of brain plasticity in pediatric patients. © 2013 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Motor dysfunction in pediatric patients with cerebral abnormalities is closely associated with corticospinal tract (CST) injury [3]. The prognosis of motor outcome is strongly correlated with the extent of CST injury [2,8], and recovery of a damaged CST is known to correspond with improvement in motor function [28]. Therefore, evaluation of CST state in pediatric patients is important in the clinical field. It provides invaluable information, especially when it is uncertain whether their delayed motor performance is

∗ Corresponding author at: Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, 317-1, Daemyungdong, Namku, Taegu 705-717, Republic of Korea. Tel.: +82 53 620 4682; fax: +82 53 625 3508. E-mail address: [email protected] (S.M. Son). 0304-3940/$ – see front matter © 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neulet.2013.10.047

pathologic or physiologic, because it allows us to make an early diagnosis. This early diagnosis enables establishment of a more detailed therapeutic strategy and commencement of early rehabilitative therapy in pediatric patients, and prevention of clinical deterioration and improvement of prognosis is very important for patients [16]. Many studies using brain ultrasonography (US), computed tomography (CT), and various magnetic resonance imaging (MRI) techniques have been attempted for detailed assessment of the CST. However, these modalities have often failed to reveal the cause of motor dysfunction in pediatric patients and to provide detailed information [1,21]. Despite development of neuroimaging, some pediatric patients showed severe motor and cognitive dysfunction even with normal MRI [15]. Diffusion tensor imaging (DTI) allows for detailed evaluation of the state of white matter tracts by virtue of its ability to image

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water diffusion characteristics [19,29]. DTI provides reproducible quantitative results, such as fractional anisotropy (FA) or apparent diffusion coefficient (ADC) [18,22]. Because of its high inherent sensitivity to changes in tissue architecture (i.e., macromolecular, cellular, tissue, and organ structure), FA is used in monitoring of structural changes in development and recovery of pathology as well as assessment of the severity of damaged white matter fibers [18,22]. In addition, diffusion tensor tractography (DTT), derived from DTI, enables three-dimensional visualization of the architecture and integrity of white matter fibers [4,17,19]. Therefore, DTT is being used increasingly in detection of CST lesions in pediatric patients with motor dysfunction [2,3,8,26,28]. In the current study, using DTI, we attempted to investigate CST recovery in pediatric hemiplegic patients and to demonstrate plastic change in immature pediatric brain after rehabilitative therapy. 2. Materials and methods 2.1. Subjects 29 patients were recruited according to the following criteria: (1) hemiplegic patients diagnosed by a pediatric neurologist; (2) initial DTI evaluation at an age ≤18-months old; (3) follow up DTI of 6–12 months duration; (4) regular physical and occupational therapy administered twice per week by experienced therapists; (5) absence of severe mental retardation, epilepsy, chromosomal anomaly, or genetic syndrome; (6) no previous history of trauma or surgery. Patients who had undergone operative procedures on their brain or extremities during follow up were also excluded. These 29 were selected from 108 patients who underwent initial DTI evaluation at an age ≤18-months old. Of the 108 children, 53 children who had undergone a follow up DTI were originally selected, and, of these 53, 18 were excluded for their follow up duration of over 12 months. Of the remaining 35, one patient was excluded for chromosomal anomaly and two patients who did not receive regular rehabilitative therapy were excluded. The other three patients admitted to the pediatric department due to intractable epilepsy were also excluded. At initial and follow up, patients underwent detailed neurologic evaluation, including gross motor function by the same pediatric neurologist. Informed consent was obtained from the parents of all participants, and the study was approved by the institutional review board at Yeungnam university hospital. 2.2. Gross motor function For evaluation of clinical gross motor functional level, the gross motor function measure (GMFM) was used at initial and follow up evaluation simultaneously with the DTI assessment. GMFM is a well established referenced measure and is widely used for interval change assessment of gross motor function in cerebral palsied patients [23,24]. There are 88 items of five sub-domains, (1) lying and rolling (17 items), (2) sitting (20 items), (3) crawling and kneeling (14 items), (4) standing (13 items), and (5) walking, running, and jumping (24 items). GMFM is scored using a 4-point ordinal scale for child’s performance level on each item. Total score is a mean score of added score number for each domain’s score. The GMFM total score ranges from 0 to 100. 2.3. DTI and diffusion tensor tractography DTIs were acquired using a sensitivity-encoding head coil on a 1.5-T Philips Gyroscan Intera system (Hoffman-LaRoche, Ltd, Best, The Netherlands) equipped with a Synergy-L Sensitivity Encoding (SENSE) head coil using single-shot echo-planar imaging and navigator echo. Sixty contiguous slices (matrix = 128 × 128; field of view = 221 × 221 mm2 ; TE = 76 mm; TR = 10,726 ms; SENSE

factor = 2; EPI factor = 67; b = 1000 s/mm/mm; NEX = 1; and slice thickness = 2.3 mm) were acquired for each of the 32 noncollinear diffusion-sensitizing gradients. Oxford Centre for Functional Magnetic Resonance Imaging of Brain (FMRIB) Software (fsl; www.fmrib.ox.ac.uk/fsl) was used for preprocessing of DTI datasets. Eddy current-induced image distortions and motion artifacts were removed using affine multi-scale two-dimensional registration. Fiber connectivity was evaluated using Fiber Assignment by Continuous Tracking (FACT), a three dimensional fiber reconstruction algorithm in Philips PRIDE software (Philips Medical Systems, Best, The Netherlands). CST fiber tracking was performed using a fractional anisotropy (FA) threshold of >0.2 and a direction threshold of 45◦ . In each case, a seed region of interest (ROI) was drawn in the CST portion of the anterior mid-pons on a 2D FA color map, and another ROI was drawn in the CST portion of the anterior low-pons on a 2D FA color map. Fiber tracts passing through both ROIs were designated as final tracts of interest. FA and ADC of depicted CSTs were determined. The mean values of FA and ADC of the entire CST were measured. The patients were classified into three groups according to the CST integrity of the contralateral hemisphere to the hemiplegia. 2.4. Statistical analysis Statistical analysis was performed in two steps. In the first step, DTI parameters of both hemispheres were compared using paired t-test. Initial and follow up data were also compared. We evaluated the significance of asymmetric differences of initial and follow up data. Degree of asymmetry between the right and left CSTs was determined by dividing the absolute difference between the means of the two sides by the means of the two sides. Relative asymmetry values were calculated using the equation: [(FA value of the more affected hemisphere − FA value of the less affected hemisphere)/((FA value of the more affected hemisphere + FA value of the less affected hemisphere)/2) × 100]. This was calculated for asymmetric anisotropy indices (AA) of CSTs at initial and follow up. The paired t-test was used for comparison of AA of initial and follow-up. In the second step, Pearson’s coefficient correlation was used for analysis of correlation between AA and each FA value of the more affected CST or less affected CST. Correlation between AA and the interval change of CST integrity was also analyzed. Correlation analysis of clinical parameter of GMFM with DTI parameters, such as FA, ADC, and AA values, was performed. Correlation analysis of CST integrity with GMFM, FA and ADC was performed using one-way analysis of variance (ANOVA). Statistical significance was accepted for p values of 0.05). In comparison of FA values between initial and follow up evaluation, follow up FA value showed a significant increase, compared with the initial result on both the more affected and less affected sides (p < 0.05). However, interval change of FA value showed a significant increase on the more affected side, compared with the less affected side (p < 0.05). Comparison of ADC showed no definite significant difference between initial and follow up values (p > 0.05). Mean AA value showing asymmetry between the more and less affected hemispheres showed a significant decrease, from 6.92 at initial to 2.28 at follow up (p < 0.05). This interval change of AA showed significant correlation with more affected FA changes (r = 0.543, p < 0.05), but no correlation with less affected FA changes (r = −0.081, p > 0.05). According to the CST integrity of the contralateral hemisphere to the hemiplegia, the patients were classified into three groups: type A; CST showed disruption at the brain stem level, type B; CST showed disruption at the corona radiata level, and type C; CST showed preserved integrity to the cortex level but decreased fiber density compared to the opposite side (Fig. 1). For integrity of the less affected CST, all patients showed preserved integrity to the cortex level and no disruption at initial and follow up evaluation. However, more affected CSTs showed disrupted integrity or decreased fiber density compared to the opposite side.

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According to the CST integrity of the more affected side, seven patients belonged to type A, 14 to type B, and eight to type C at the initial evaluation. However, at the follow up evaluation, no patients belonged to type A, six patients to type B, and 23 to type C. In other words, four patients changed from type A to B, three patients changed from type A to C, and 12 patients changed from type B to C. This change in integrity showed significant correlation with changes of AA (r = 0.469, p < 0.05). There was no significant difference was observed in the correlation of CST type with FA, ADC and GMFM (p > 0.05). GMFM showed no significant correlation with DTT parameters, including FA, ADC, AA, and CST integrity (p > 0.05). 4. Discussion In the current study, we investigated CST recovery after rehabilitative treatment in hemiplegic pediatric patients using DTI. For the following reasons, we believe that the hemiparesis of our patients was caused by the affected CST, and their clinical improvement was due to the recovery of that affected CST. First, CST of the contralateral hemisphere to the hemiplegic side in the patients showed significantly decreased FA values compared with the opposite side. An injured CST, which has different diffusion characteristics, often shows decreased FA value [6,14,20,26]. Several studies using DTI have investigated CST lesions in pediatric patients with motor dysfunction. Murakami et al. [20] reported significantly decreased FA of the lesional side CST in hemiparetic cerebral palsied patients with periventricular white matter injury compared with those of controls. Another study by Son et al. [26] reported significantly decreased FA value and disrupted integrity of the affected CST in hemiparetic cerebral palsied patients who did not show an abnormal brain lesion on conventional MRI. In the current study, all hemiplegic patients also showed significantly decreased FA value of the more affected CST compared to the less affected CST. In addition, 18 of 29 patients who had no explainable lesion on conventional MRI regarding their clinical hemiparesis also showed significantly decreased FA value of the CST corresponding to the clinical symptom. These results, which were concordant with those of previous studies, suggest that DTI is very sensitive for detection of CST abnormalities in pediatric hemiplegic patients regardless of brain lesion on conventional MRI, and that the CSTs of the hemisphere contralateral to the hemiparetic side in our patients were affected. Second, a significant decrease in AA was observed at the follow up evaluation compared to the initial value. AA represents severity of injury of the affected CST against the unaffected side quantitatively [7,9,26,27]. In several previous studies, AA has been used as a sensitive measure for assessment of the severity of CST lesions. Glenn et al. [9], who researched difference between congenital hemiparetic patients and age-matched control subjects using AA, reported significantly higher AA of the pyramidal tract in hemiparetic patients, compared with control subjects. Findings of another comparative study between hemiplegic and diplegic cerebral palsied patients with symmetric periventricular leukomalacia

Table 2 Comparison of FA, ADC, AA, and GMFM of initial and follow up study. FA

Initial FU

ADC

Affected CST

Unaffected CST

Affected CST

Unaffected CST

0.426 (0.037) 0.470† (0.027)

0.456* (0.032) 0.481* , † (0.028)

0.950 (0.065) 0.901 (0.092)

0.940 (0.049) 0.920 (0.059)

AA

GMFM

6.92 (5.24) 2.28† (3.06)

27.59 (17.00) 72.34† (15.28)

Values are expressed as mean (±standard deviation), FA: fractional anisotropy, ADC: apparent diffusion coefficient, AA: asymmetric anisotropy, GMFM: gross motor function measure, CST: corticospinal tract, FU: follow up. * Significantly different compared to the opposite side at p < 0.05. † Significantly different compared to the initial evaluation at p < 0.05.

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Fig. 1. Conventional magnetic resonance image (MRI) and diffusion tensor image (DTI). Patients were classified into three groups according to the more affected corticospinal tract (CST). (A) T2-weighted brain MRI, (B) DTI of the CST (right CST: red color, left CST: yellow color, R: right): type A; disrupted CST at the brain stem level, type B; disrupted CST at the corona radiata level, and type C; preserved integrity of CST to the cortex level but decreased fiber density compared to the opposite side. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)

revealed significantly higher AA in the hemiplegic group than in the diplegic group [7]. Increased AA values in these previous results signify asymmetric CST lesion between both hemispheres in patients. In this study, our patients showed a significant decrease of follow up AA value after rehabilitative treatment with improvement of clinical hemiparesis compared to the initial evaluation. This means that the asymmetry between more and less CSTs states was reduced. In addition, interval changes of FA of the more affected CST were significantly larger than those of the less affected CST. AA interval change showed significant correlation with FA interval change of the more affected CST, not with the less affected CST. These results imply that a decrease of AA at follow up is related to the decrease of injury severity of the more affected CST rather than interval change of the less affected CST in our patients. This is likely to be associated with rehabilitative treatment, which focuses more on the more affected side rather than the less affected side. Third, CST of the more affected side showed greater disruption than that of the less affected CST, and the disruption of the more affected CST showed improvement at the follow up evaluation. No studies on interval changes of a disrupted CST in pediatric patients using DTI have been reported, however, a few studies in stroke patients have been reported [10–13]. Jang et al. [10] reported recovery of a partially damaged CST in a patient with intracerebral hematoma using follow up DTT. Another DTI study on longitudinal changes of an injured CST in stroke patients reported that 14 of 45 patients (31%) patients showed change in integrity of disrupted CSTs [13]. In the current study, 66% of patients also showed radiologic improvement, which showed change of integrity of the more affected CST. We believe that the patient’s hemiplegic extremities were influenced more by rehabilitative treatment than the opposite side. Absolutely, both CSTs of the more affected and less affected sides in our patients underwent maturation during the study period.

However, due to rehabilitative treatment, the therapeutic effect as well as maturational effect might have been greater for the more affected side, compared with the less affected side. Usually, pediatric brains, which are still immature, undergo rapid maturation until postnatal 24 months and then gradually until 132 months [25]. Despite a relatively short study period, we think that patients in this study who were younger than 24 months would show greater change. Previous studies have reported on use-dependent plasticity upon the affected motor fiber tract [5,30]. Bengtsson et al., who investigated experience-dependent plasticity, reported change of motor fiber tracts through extensive piano practice [5]. Another study on experience dependent plasticity showed CST changes in men with early blindness [30]. These results suppose that experience-dependent plasticity through rehabilitative therapy would have an influence on our patient, especially on the more affected side. In this study, we used DTI to demonstrate recovery of the CST in pediatric patients. The authors believe that these results have important implications for the scientific basis of brain plasticity in the immature pediatric brain. However, this study is limited by a small number of patients due to strict inclusion criteria. The young age of subjects, whose brain diffusivity has strong time dependence due to rapidly ongoing myelination, can be another limitation [25]. Because the subjects were so young, the complete examination for visual acuity, whole EMG/NCV examination to rule out the possibility of abnormal peripheral nerve system, and an MRI examination of the spinal cord could not be performed in all participants. We also could not exclude bony torsion or asymmetry using CT evaluation, which could cause motor impairment, although none of the patients showed muscle and joint contractures. In addition, detailed clinical data could not be obtained due to young and various distributions of ages in patients; we think that this may lead to insignificant results

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between clinical GMFM changes and radiologic changes. This various age distribution may also lead to insignificant result between CST type and GMFM score or DTI parameters. Therefore, conduct of further complementary studies involving larger case numbers and more detailed clinical parameters is warranted. Acknowledgements This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2012-013997). References [1] P.Y. Ancel, F. Livinec, B. Larroque, S. Marret, C. Arnaud, V. Pierrat, M. Dehan, S. N’Guyen, B. Escande, A. Burguet, G. Thiriez, J.C. Picaud, M. Andre, G. Breart, M. Kaminski, E.S. Grp, Cerebral palsy among very preterm children in relation to gestational age and neonatal ultrasound abnormalities: the EPIPAGE cohort study, Pediatrics 117 (2006) 828–835. [2] Y. Arzoumanian, M. Mirmiran, P.D. Barnes, K. Woolley, R.L. Ariagno, M.E. Moseley, B.E. Fleisher, S.W. Atlas, Diffusion tensor brain imaging findings at term-equivalent age may predict neurologic abnormalities in low birth weight preterm infants, Am. J. Neuroradiol. 24 (2003) 1646–1653. [3] B.Q. Banker, J.C. Larroche, Periventricular leukomalacia of infancy. A form of neonatal anoxic encephalopathy, Arch. Neurol. 7 (1962) 386–410. [4] P.J. Basser, C. Pierpaoli, Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI, J. Magn. Reson. Ser. B 111 (1996) 209–219. [5] S.L. Bengtsson, Z. Nagy, S. Skare, L. Forsman, H. Forssberg, F. Ullen, Extensive piano practicing has regionally specific effects on white matter development, Nat. Neurosci. 8 (2005) 1148–1150. [6] M.C. Chang, S.H. Jang, S.S. Yoe, E. Lee, S. Kim, D.G. Lee, S.M. Son, Diffusion tensor imaging demonstrated radiologic differences between diplegic and quadriplegic cerebral palsy, Neurosci. Lett. 512 (2012) 53–58. [7] H.K. Cho, S.H. Jang, E. Lee, S.Y. Kim, S. Kim, Y.H. Kwon, S.M. Son, Diffusion tensor imaging-demonstrated differences between hemiplegic and diplegic cerebral palsy with symmetric periventricular leukomalacia, Am. J. Neuroradiol. 34 (2013) 650–654. [8] A. Drobyshevsky, J. Bregman, P. Storey, J. Meyer, P.V. Prasad, M. Derrick, W. MacKendrick, S. Tan, Serial diffusion tensor imaging detects white matter changes that correlate with motor outcome in premature infants, Dev. Neurosci. (Basel) 29 (2007) 289–301. [9] O.A. Glenn, R.G. Henry, J.I. Berman, P.C. Chang, S.P. Miller, D.B. Vigneron, A.J. Barkovich, DTI-based three-dimensional tractography detects differences in the pyramidal tracts of infants and children with congenital hemiparesis, J. Magn. Reson. Imaging 18 (2003) 641–648. [10] S.H. Jang, W.M. Byun, B.S. Han, H.J. Park, D. Bai, Y.H. Ahn, Y.H. Kwon, M.Y. Lee, Recovery of a partially damaged corticospinal tract in a patient with intracerebral hemorrhage: a diffusion tensor image study, Restor. Neurol. Neurosci. 24 (2006) 25–29. [11] S.H. Jang, S.H. Kim, S.H. Cho, B.Y. Choi, Y.W. Cho, Demonstration of motor recovery process in a patient with intracerebral hemorrhage, Neurorehabilitation 22 (2007) 141–145.

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CST recovery in pediatric hemiplegic patients: Diffusion tensor tractography study.

Many diffusion tensor imaging (DTI) studies have reported an association between corticospinal tract (CST) injury and motor dysfunction. In this study...
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