Int. J. Devl Neuroscience 34 (2014) 42–47

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International Journal of Developmental Neuroscience journal homepage: www.elsevier.com/locate/ijdevneu

Assessing sequence and relationship of regional maturation in corpus callosum and internal capsule in preterm and term newborns by diffusion-tensor imaging XiaoLin Miao a,1 , Min Qi b,1 , ShuDong Cui a,∗ , YaFei Guan a , ZhenYu Jia b , XunNing Hong b , YanNi Jiang b a b

Department of Pediatrics, The First Affiliated Hospital of Nanjing Medical University, Jiangsu 210029, China Department of Radiology, The First Affiliated Hospital of Nanjing Medical University, Jiangsu 210029, China

a r t i c l e

i n f o

Article history: Received 16 August 2013 Received in revised form 23 December 2013 Accepted 18 January 2014 Keywords: White matter maturation FA ADC Brain development

a b s t r a c t Background: Diffusion-tensor imaging (DTI) can be used to investigate water diffusion in living tissue. Objective: To investigate sequence and relationship of regional maturation in corpus callosum (CC) and internal capsule (IC) in preterm and term. Methods: DTI was performed on 11 preterm infants at less than 37 weeks of corrected gestational age (group I), 21 preterm infants at equivalent-term (group II), 11 term infants during neonatal period (group III). Apparent diffusion coefficient (ADC) and fractional anisotropy (FA) were measured in: anterior limb of IC (ALIC), posterior limb of IC (PLIC), genu and splenium of CC. Results: FA in splenium was more than that in other regions except genu of group I. Differences of FA between genu and PLIC were significant only in group III. ADC in genu was more than that in other regions but in splenium of groups I and II. Differences of ADC between splenium and ALIC were insignificant except group II. Higher FA and lower ADC in PLIC were gotten compared with those in ALIC. Correlations of FA and of ADC existed in CC and IC. Conclusion: Maturation sequence was splenium followed by genu, then by PLIC and last by ALIC in term at neonatal period. Genu’s maturation in preterm at equivalent-term was hindered. Regional maturation’s correlations existed in CC and IC. © 2014 ISDN. Published by Elsevier Ltd. All rights reserved.

1. Introduction White matter injury (WMI) is an important problem in premature infants of between 24 and 34 weeks of birth gestational age (GA) (Jensen, 2006), which results in disrupted white matter (WM) maturation and chronic myelination disturbances (Volpe, 2008). To understand WMI in preterm infants requires continued efforts on understanding the underlying microstructural changes in brain development, especially the maturation of white matter, in preterm. The development of white matter myelination in the preterm has been described qualitatively by conventional MRI (Counsell et al., 2002). To assess accurately the microstructural changes during maturation in preterm brain needs a non-invasive, “in vivo” assessment of white matter development quantitatively. Diffusion-tensor imaging (DTI) offers great potential to fulfill the

∗ Corresponding author at: Department of pediatrics, The First Affiliated Hospital of Nanjing Medical University, Jiangsu 210029, China. Tel.: +86 13770687101. E-mail address: [email protected] (S. Cui). 1 These authors contributed equally to this study. 0736-5748/$36.00 © 2014 ISDN. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijdevneu.2014.01.004

need. DTI can be used to investigate diffusion properties of water in living tissue (Mathur et al., 2010), which is a useful tool of studying white matter maturation and injury during childhood (Jiao et al., 2010; Welker and Patton, 2012). Fractional anisotropy (FA) describes the degree to which water diffusion is restricted in one direction relative to others, ranging from 0 to 1, with 0 being completely isotropic diffusion and 1 being diffusion constrained in one direction only. In mature white matter, water diffusion is highly anisotropic in that water molecules move less freely perpendicular to fibers than parallel to them. During development, the increase of FA in white matter appears to occur in three stages (Dubois et al., 2008). First stage, fiber organization occurs, during which anisotropy exists in white matter in late intrauterine and premature infants (Kostovic and Jovanov-Milosevic, 2006). The increase of anisotropy seems to correlate with the developmental expansion of immature oligodendrocytes during the premyelination period (Drobysehvsky et al., 2005). Second stage, maturation of pre- and immature oligodendroglial cells, as well as the development of the cytoskeleton and various intracellular structures. Third stage, myelination, which is associated with histological appearance of myelin and its maturation around axons (Wozniak and Lim, 2006;

X. Miao et al. / Int. J. Devl Neuroscience 34 (2014) 42–47

Taki and Kawashima, 2012). So the increase of FA is closely related to the maturation of white matter. We used FA as an indication of white matter maturation just like that Klingberg et al. (1999) and Colby et al. (2011) did. Apparent diffusion coefficient (ADC), which reflects the rate of microscopic water motion in a regional tissue, is used to evaluate water content and to a lesser degree to evaluate white matter myelination (Provenzale et al., 2007). We designed this study to detect and analyze FA and ADC in corpus callosum (CC) and internal capsule (IC) of three groups’ infants, who were preterm infants at less than 37 weeks of corrected GA, at equivalent-term, and term infants at neonatal period. Our aims were: (1) to study differences of regional maturation in CC and IC in preterm and term, (2) to study whether FA and ADC in CC and IC in preterm at equivalent-term can catch up with those in term, (3) to investigate relationships of regional FA and ADC in CC and IC. 2. Materials and methods 2.1. Subject selection From October of 2010 to January of 2013, we collected 32 cases of preterm babies, who were hospitalized in neonatal department of the first affiliated hospital of Nanjing Medical University, whose parental consents were gotten, whose birth GA was from 27.4 weeks to 34.5 weeks (median: 32.3 weeks), among whom 15 cases’ birth GA was from 27.4 weeks to 32 weeks and 17 cases’ birth GA was between 32.2 weeks and 34.5 weeks. There were 22 boys and 10 girls, whose birth weight (BW) was from 840 to 2900 g (median: 1550 g). During this period, there were 11 cases of hospitalized term babies, who should be examined MRI for clinical diagnoses and whose parental consents were gotten, among whom 3 cases were because of cephalohematoma, 3 cases because of SGA, 2 cases because of meconium aspiration syndrome, 2 cases because of newborn sepsis, 1 case because of benign familial neonatal seizures, 4 girls and 7 boys, whose BW was between 2050 and 4000 g. Inclusion criteria: (1) parental consents were gotten, (2) infants needed to receive conventional MRI for clinical diagnoses, (3) conventional MRI imaging of brain were normal (if the babies’ parental consents were not gotten, they just received conventional MRI). Exclusion criteria: (1) infants were suffered from severe intracranial hemorrhage, white matter injury, brain infarct, neonatal meningitis, or congenital anomaly, (2) infants need not receive conventional MRI for clinical diagnoses, (3) parental consents were not gotten. GA was calculated from the date of last menstrual period and was confirmed with early prenatal ultrasound scanning. The research ethics committee of the first affiliated Hospital of Nanjing Medical University approved the study, and the informed parental consents were obtained. 2.2. Groups and methods 2.2.1. Groups Preliminarily, we designed to divide the enrolled preterm babies into two groups, but some babies lived too far from our hospital and some babies’ parents had no time to come back to our hospital by the due date, so we let the enrolled babies’ parents choose when the babies came back. Finally we were not able to randomly separate the preterm babies into two groups. Group I, 11 preterm infants were done DTI at less than 37 weeks of corrected GA (BW: 1568 ± 308 g, GA: 30.9 ± 1.5 weeks), group II, 21 preterm infants, on whom DTI was performed at equivalent-term age (BW: 1680 ± 555 g, GA: 32.0 ± 2 weeks); There was no difference in GA (p = 0.174) and BW (p = 0.54) between groups I and II. Group III, 11 term infants were done DTI during the neonatal period. 2.2.2. Preparations for infants DTI was performed on the infants when their vital signs were stable. Infants were sedated with orally administered chloral hydrate (50 mg/kg). Before sedating infants, we checked whether there was metal on the infants or not, and took measurements of hearing protection. Patients should be wrapped snugly in 1–2 sheets. 2.2.3. Imaging parameters A MRI protocol was performed on the subjects with a 3.0-Tesla MRI scanner (Trio, Siemens, Germany). The MRI protocol included a T1-weighted sequence, a T2-weighted sequence, a FLAIR sequence, and a DTI sequence. As the number of gradient directions increases, the quality of FA maps becomes better, while imaging needs longer time and the number of artifacts increase for newborn babies. Basser et al. reported that minimum of six gradient directions are necessary to assess diffusion anisotropy fully (Basser and Pierpaoli, 1996). Some researchers just used 6 directions in their studies (Colby et al., 2011; Provenzale et al., 2012; Cheong et al., 2009). In this study, DTI images were acquired in the axial plane with a 12-direction diffusion weighted multi-slice echoplanar spin-echo imaging protocol, TR = 3000 ms, TE = 93 ms, slice thickness = 4 mm, inter-slice gap = 0.4 mm, voxel

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Table 1 Regional ADC and FA values in CC and IC of three groups. I Genu of CC 1.542 ADC FA 0.435 Splenium of CC 1.504 ADC FA 0.518 ALIC (right) 1.330 ADC 0.263 FA PLIC (right) 1.138 ADC 0.397 FA ALIC (left) 1.328 ADC 0.390 FA PLIC (left) 1.121 ADC 0.226 FA

II

III

± 0.159 ± 0.080

1.416 ± 0.164 0.513 ± 0.105

1.329 ± 0.147 0.589 ± 0.064

± 0.427 ± 0.137

1.336 ± 0.303 0.673 ± 0.126

1.163 ± 0.073 0.694 ± 0.071

± 0.089 ± 0.040

1.171 ± 0.100 0.331 ± 0.057

1.137 ± 0.063 0.320 ± 0.050

± 0.102 ± 0.059

1.032 ± 0.069 0.477 ± 0.070

1.002 ± 0.041 0.477 ± 0.065

± 0.073 ± 0.051

1.151 ± 0.090 0.481 ± 0.082

1.122 ± 0.052 0.503 ± 0.053

± 0.091 ± 0.039

1.028 ± 0.074 0.298 ± 0.048

1.009 ± 0.049 0.302 ± 0.042

Mean ± SD (ADC × 10−5 mm2 /s). size 1.9 mm × 1.8 mm × 3.0 mm, average = 1, b-value = 1000 s/mm2 . All images were processed on workstation of Syngo MR1317 (Siemens, Germany). Using Functional software, the analysts blinded to any clinical material drew regions of interest in anterior limb of IC (ALIC), posterior limb of IC (PLIC) of the left and the right, genu and splenium of CC on ADC and FA maps with reference to corresponding T2-weighted images, and measured ADC and FA. In group II, there were artifacts on ALIC of the left in one case (the data in ALIC of this case were deleted). 2.3. Statistical analyses Data were analyzed with SPSS16 software (StatsDirect, Sale, United Kingdom). ADC and FA values were showed up with equivalence ± SD for groups. Comparisons of regional FA and ADC values and of different group’s FA and ADC were analyzed by independent-samples t test. Relationship of regional FA and ADC was analyzed by correlation analysis. The results were significant at a level of p < 0.05.

3. Results 3.1. ADC and FA values ADC and FA values (mean ± SD) in genu and splenium, in ALIC (of the right and of the left) and PLIC (of the right and of the left) of three groups were showed in Table 1. Fig. 1 showed the images of CC and IC on DTI in three groups. 3.2. Comparisons of regional FA in three groups FA values in splenium were the highest among those in all measured regions in each group, and the differences of FA were significant statistically between splenium and other regions except genu of group I (p = 0.098). The differences of FA between genu and PLIC (of the right and of the left) were not significant statistically in groups I and II, but in group III. The differences of FA between PLIC (of the right and of the left) and ALIC (of the right and of the left) were significant statistically in three groups (p values see Table 2). We rebuilt 3-dimensional images of fiber bundles in CC and IC of three groups, respectively, from which we can see that the density and the number of fiber bundles in splenium were more than those in genu in three groups, and that the density and the number of fiber bundles in PLIC were more than those in ALIC in three groups (see Fig. 2). 3.3. Comparisons of regional ADC in three groups ADC in genu was more than that in other regions measured in each group, except splenium of group I (p = 0.781) and of group II (p = 0.298). The differences of ADC between splenium and ALIC (of

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X. Miao et al. / Int. J. Devl Neuroscience 34 (2014) 42–47

Fig. 1. 1A, 1B showed fractional anisotropy maps of IC and CC of one case from group I, 2A, 2B showed fractional maps of IC and CC of one case from group II, 3A, 3B showed fractional maps of IC and CC of one case from group III. 1C, 2C, 3C showed apparent diffusion coefficient maps of IC and CC from groups I, II, III, respectively.

Table 2 p Values and 95% CI of difference of comparisons of regional FA in CC and IC of three groups. FA Splenium of CC I II III ALIC (right) I II III PLIC (right) I II III ALIC (left) I II III PLIC (left) I II III

Genu of CC

Splenium of CC

ALIC (right)

PLIC (right)

ALIC (left)

0.098 (−0.182 to 0.017) 0.000 (−0.232 to −0.088) 0.002 (−0.166 to −0.045) 0.000 (0.117 to 0.229) 0.000 (0.129 to 0.235) 0.000 (0.218 to 0.320)

0.000 (0.162 to 0.350) 0.000 (0.280 to 0.404) 0.000 (0.320 to 0.429)

0.215 (−0.024 to 0.101) 0.194 (−0.019 to 0.092) 0.001 (0.054 to 0.169)

0.018 (0.024 to 0.218) 0.000 (0.132 to 0.261) 0.000 (0.157 to 0.278)

0.000 (−0.180 to −0.090) 0.000 (−0.186 to −0.106) 0.000 (−0.209 to −0.106)

0.000 (0.154 to 0.266) 0.000 (0.163 to 0.267) 0.000 (0.239 to 0.335)

0.000 (0.199 to 0.387) 0.000 (0.314 to 0.436) 0.000 (0.341 to 0.444)

0.042 (0.002 to 0.072) 0.054 (−5.235 to 0.067) 0.374 (−0.023 to 0.059)

0.000 (0.127 to 0.216) 0.000 (0.141 to 0.217) 0.000 (0.126 to 0.224)

0.132 (−0.015 to 0.104) 0.277 (−0.027 to 0.090) 0.003 (0.034 to 0.138)

0.013 (0.032 to 0.223) 0.000 (0.125 to 0.259) 0.000 (0.135 to 0.247)

0.000 (−0.169 to −0.087) 0.000 (−0.194 to −0.106) 0.000 (−0.229 to −0.137)

0.783 (−0.043 to 0.056) 0.851 (−0.052 to 0.043) 0.319 (−0.079 to 0.027)

the right and of the left) were not significant in group I (p = 0.212, 0.206 separately) and III (p = 0.387, 0.142 separately), but in group II. ADC in ALIC was more than that in PLIC in each group (p values see Table 3).

0.000 (−0.206 to −0.124) 0.000 (−0.226 to −0.141) 0.000 (−0.244 to −0.159)

3.4. Comparisons of ADC and FA between different groups ADC values in group I were more than those in group II and III, and the differences were significant statistically, except in

Fig. 2. 1A, 2A, 3A showed 3-dimension maps of IC and CC in groups I, II, III, respectively. The number and the density of fiber bundles in splenium were more than those in genu by comparing 1C with 1B, 2C with 2B, 3C with 3B. The number and the density of fiber bundles in PLIC were more than those in ALIC by 1D, 2D and 3D (1 = group I, 2 = group II, 3 = group III. B, C, D represented genu, splenium, internal capsules respectively).

X. Miao et al. / Int. J. Devl Neuroscience 34 (2014) 42–47

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Table 3 p Values and 95% CI of difference of comparisons of regional ADC in CC and IC of three groups. ADC Splenium of CC I II III ALIC (right) I II III PLIC (right) I II III ALIC (left) I II III PLIC (left) I II III

Genu of CC

Splenium of CC

ALIC (right)

PLIC (right)

ALIC (left)

0.781 (−0.248 to 0.326) 0.298 (−0.074 to 0.233) 0.003 (0.063 to 0.269) 0.001 (0.098 to 0.328) 0.000 (0.160 to 0.330) 0.001 (0.088 to 0.295)

0.212 (−0.116 to 0.465) 0.025 (0.022 to 0.309) 0.387 (−0.035 to 0.086)

0.000 (0.286 to 0.524) 0.000 (0.304 to 0.463) 0.000 (0.226 to 0.427)

0.018 (0.075 to 0.658) 0.000 (0.164 to 0.444) 0.000 (0.108 to 0.214)

0.000 (0.107 to 0.277) 0.000 (0.085 to 0.192) 0.000 (0.088 to 0.182)

0.001 (0.105 to 0.325) 0.000 (0.181 to 0.348) 0.001 (0.106 to 0.309)

0.206 (−0.113 to 0.465) 0.013 (0.042 to 0.327) 0.142 (−0.015 to 0.098)

0.962 (−0.0707 to 0.074) 0.520 (−0.041 to 0.080) 0.533 (−0.036 to 0.067)

0.000 (−0.269 to −0.112) 0.000 (−0.170 to −0.069) 0.000 (−0.161 to −0.078)

0.000 (0.306 to 0.537) 0.000 (0.308 to 0.469) 0.000 (0.219 to 0.422)

0.014 (0.093 to 0.673) 0.000 (0.168 to 0.450) 0.000 (0.099 to 0.210)

0.000 (0.128 to 0.289) 0.000 (0.088 to 0.198) 0.000 (0.078 to 0.179)

0.693 (−0.069 to 0.102) 0.835 (−0.040 to 0.050) 0.738 (−0.047 to 0.034)

splenium (p = 0.207 group I vs II). FA values in group I were less than those in group II and III, and the differences were significant statistically. The differences of FA and ADC values between groups II and III were not significant statistically in all measured regions, except ADC in splenium (p = 0.020) and FA in genu (p = 0.038) (p values see Table 4). 3.5. Relationships of regional FA and of regional ADC in CC and IC of all studied infants There were relationships of FA and of ADC between splenium and genu, ALIC and PLIC, whatever of the left and of the right, between CC and IC, except between splenium and PLIC. The correlation coefficient (R) of intra-IC was more than that of intra-CC (R and p values see Tables 5 and 6). 4. Discussion We showed that FA in splenium was more than that in genu in each group. The difference was not statistically significant in preterm infants at less than 37 corrected GA (p = 0.098), but in preterm at term-equivalent and in term (p = 0.000/0.002). It seemed to suggest that the maturation in splenium was prior to that in genu in preterm at term-equivalent and in term. FA in genu was more than that in PLIC (including right and left), the difference was not significant in preterm at less than 37 corrected GA (p = 0.215/0.132, right and left separately) and at equivalent-term (0.194/0.277, right and left separately), but in term. It suggested that in term, maturation in genu was prior to that in PLIC, and in preterm infants at equivalent-term, maturation in genu could be hindered. FA in PLIC, whatever of the right and of the left, was more than that in ALIC in three groups. From above, we may deduced that maturation sequence was that splenium followed by genu, then by PLIC and last by ALIC in term. Maturation in genu in preterm at equivalentterm was hindered. Because we did not stratify the population of preterm to decrease the influence of such factors as ventilation, GA, and pathologies of prematurity other than CNS disease, we do not differentiate what caused the hinderance of maturation in genu in preterm was from in-uterine factors or out-uterine factors. Histological studies (Yakovlev and Lecours, 1967) have demonstrated that myelination in IC can be demonstrated from the ninth fetal month, much earlier than myelination in the CC. There seems to be contradictory with our results. Kinney’s study (Kinney et al., 1988) shows that there is variability in the timing of myelination within

0.00 (0.134 to 0.280) 0.000 (0.072 to 0.176) 0.000 (0.068 to 0.158)

and across axonal systems, and early onset of myelination is not always followed by early myelin maturation. We think early onset of maturation is not always followed by early myelin maturation. We rebuilt 3-dimensional images of fiber bundles in CC and IC of three groups, respectively, from which we can see that the density and the number of fiber bundles in splenium were more than those in genu in three groups, and that those in PLIC were more than in ALIC in three groups, but just from which it was difficult for us to decide that those were more in genu or in PLIC. A study (Partridge et al., 2004) was performed on 14 preterm newborns imaged between 28 and 39 weeks of corrected GA, which showed that no difference of FA existed between splenium and genu, genu and PLIC. The reasons of the difference between ours and theirs could be that they did not separate the infants into different groups, and the span of imaged corrected GA was different from ours. We also compared regional ADC in three groups. ADC in genu was the highest among that in these regions, and the difference of ADC was significant between in genu and in other regions except splenium in preterm (including at less than 37 corrected GA and at equivalent-term). The difference of ADC between in splenium and in ALIC was not significant in preterm at less than 37 corrected GA and in term, but in preterm at equivalent-term. The difference of ADC between in ALIC and in PLIC was significant in each group. From above, it indicated that the decrease of water content in splenium could be hindered in preterm at equivalent-term. This study showed that the differences of ADC and FA in CC and IC between in preterm at less than 37 weeks of corrected GA and in preterm at equivalent-term were significant generally. Namely, the general tendency of ADC and FA was that, with brain developing, ADC tended to be decreased, FA tended to be increased in CC and IC. But there was no significant difference of ADC in splenium between them (p = 0.207). The similar results are gotten in the other studies. Dudink et al. (Dudink et al., 2008) reported that after 30 weeks GA, in fetuses, preterm neonates and term neonates, ADC values progressively decreased. Miller et al. (Miller et al., 2002) demonstrated that ADC decreased and anisotropy increased with age in newborns. The similar results (Provenzale et al., 2007) were also reported during the first year of life, even myelination is completed (Utsunomiya, 2011). In white matter, developmental decrease in ADC and increase in FA reflect the process of white matter maturation (Dubois et al., 2008), such as ‘premyelinating state’ (Huppi and Dubois, 2006; Back et al., 2002), myelination, water content (Mukherjee et al., 2002), cell density, formation of white

0.451 (−0.032 to 0.070) 0.438 (−0.077 to 0.034) 0.322 (−0.031 to 0.090) 0.841 (−0.0391 to 0.032) 0.195 (−0.016 to 0.077) 0.995 (−0.052 to 0.052) 0.020 (0.030 to 0.317) 0.617 (−0.105 to 0.064) II vs III

ADC FA

0.154 (−0.034 to 0.207) 0.038 (−0.146 to −0.004)

0.322 (−0.035 to 0.102) 0.571 (−0.030 to 0.053)

0.002 (0.048 to 0.178) 0.000 (−0.159 to −0.066) 0.000 (0.150 to 0.262) 0.000 (−0.112 to −0.040) 0.001 (.067 to 0.205) 0.007 (−0.135 to −0.024) 0.025 (0.05 to 0.630) 0.002 (−0.275 to −0.077) I vs III

ADC FA

0.004 (0.077 to 0.349) 0.000 (−0.218 to −0.089)

0.000 (0.124 to 0.261) 0.008 (−0.097 to −0.0167)

0.000 (0.112 to 0.241) 0.000 (−0.107 to −0.038)

ALIC (left) PLIC (right)

0.002 (.043 to 0.167) 0.003 (−0.130 to −0.029) 0.000 (0.085 to 0.232) 0.001 (−0.108 to −0.029) 0.207 (−0.098 to 0.433) 0.003 (−0.254 to −0.056) 0.045 (0.003 to 0.250) 0.039 (−0.152 to −0.004)

ALIC (right) Splenium Of CC Genu of CC

ADC FA I vs II

Table 4 p Values and 95% CI of difference of comparisons of regional ADC and FA values between different groups.

0.004 (0.033 to 0.155) 0.002 (−0.146 to −0.035)

X. Miao et al. / Int. J. Devl Neuroscience 34 (2014) 42–47

PLIC (left)

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Table 5 R and p values of correlations of regional FA in CC and IC of all studied infants. FA

Genu of CC

Splenium of CC 0.499 R p Value 0.001 ALIC (right) 0.346 R p Value 0.023 PLIC (right) 0.305 R p Value 0.047 ALIC (left) 0.417 R p Value 0.006 PLIC (left) 0.386 R p Value 0.01

Splenium of CC

ALIC (right)

PLIC (right)

ALIC (left)

0.364 0.016 0.172 0.270

0.505 0.001

0.459 0.002

0.609 0.000

0.404 0.008

0.268 0.082

0.537 0.000

0.686 0.000

0.450 0.003

R, correlation coefficient.

matter tracts, membrane potential (Schneider et al., 2007; Prayer and Prayer, 2003), maturational changes in the cytoskeletal structure of neuronal axonal cylinders and compartmentalization of WM extracellular spaces (Haynes et al., 2005). This study showed that ADC and FA values in preterm at termmatched age were generally similar to those in term at neonatal period, the differences of FA and ADC between them were not significant generally. This suggested that the developmental level in CC and IC in preterm at term-matched age could catch up with that in term. Anjari et al. (Anjari et al., 2007) reported that FA in genu in preterm at term-equivalent age was lower than that in term, and additional reductions of FA in PLIC were found in preterm at less than or equal to 28 weeks GA. Thompson et al. (Thompson et al., 2011) found that very preterm infants (

Assessing sequence and relationship of regional maturation in corpus callosum and internal capsule in preterm and term newborns by diffusion-tensor imaging.

Diffusion-tensor imaging (DTI) can be used to investigate water diffusion in living tissue...
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