Secondary Damage in Left-Sided Frontal White Matter Detected By
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Li et al. European Journal of Medical Research 2014, 19:44 http://www.eurjmedres.com/content/19/1/44 EUROPEAN JOURNAL OF MEDICAL RESEARCH RESEARCH Open Access Secondary damage in left-sided frontal white matter detected by diffusion tensor imaging is correlated with executive dysfunction in patients with acute infarction at the ipsilateral posterior corona radiata Chuo Li1*, Chao Dang2, Gang Liu2, Li Chen2, Jian Zhang2, Jingjing Li2, Zilin Ou2, Yusheng Zhang3 and Anding Xu3 Abstract Background: Executive dysfunction has been observed in patients with left-sided anterior corona radiata infarction. However, whether left-sided posterior corona radiata infarction could cause executive dysfunction is unclear. Also, whether secondary damage in the left frontal white matter following ipsilateral posterior corona radiata infarct is causal or not and contributes to the occurrence and development of executive dysfunction, is still uncertain. Methods: Twelve patients with posterior corona radiata infarction underwent diffusion tensor imaging (DTI) and an executive functional assessment at week 1 (W1), week 4 (W4), and week 12 (W12) after onset. Color duplex sonography and Transcranial Duplex Scanning (TCD) were performed at W1 and W12. Twelve healthy volunteers of similar ages and educational histories were examined as controls and assessed once. Results: In the patients, we observed an increased mean diffusivity (MD) and a decreased fractional anisotropy (FA) in the left frontal white matter from W1 to W12. There were no significant changes in cerebral blood flow in patients between W1 and W12 according to the result of Color duplex sonography and TCD. Patients showed progressively impaired executive function during 12 weeks. Significant correlations were found between increased MD and decreased FA in the left frontal white matter with impaired degree of executive function. Conclusions: This study demonstrates that DTI detected secondary damage in left-sided frontal white matter in patients with acute infarction at the ipsilateral posterior corona radiata. This change may be correlated with executive functional changes in these patients. Keywords: Cerebral infarction, Executive dysfunction, Diffusion tensor imaging Background The frontal-subcortical white matter connections as well The term ‘executive functions’ is used to describe high- as the frontal lobe are well known to be functionally crit- order cognitive processes which include control, integra- ical in the control of executive function [3]. Lesions of tion, organization and maintenance of other cognitive not only the prefrontal cortex but subcortical areas re- abilities [1]. Executive dysfunction might predict poor sult in executive dysfunction [4,5]. In particular, damage functional outcome of patients with stroke [2]. The of frontal white matter, which is an important region in frontal lobes have extensive connections with portions frontal-subcortical circuitry, results in this executive of the limbic system, the basal ganglia, and the thalamus. dysfunction [6]. Recently, accumulating studies have shown histopatho- * Correspondence: [email protected] logical and radiological changes occurring in nonischemic 1Department of Neurology, Guangzhou Number 8 People’s Hospital, remote brain regions that have synaptic connections with Guangzhou Medical University, 8, Huaying Road, Guangzhou 510440, China the primary lesion site. For example, after cerebral Full list of author information is available at the end of the article © 2014 Li et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Li et al. European Journal of Medical Research 2014, 19:44 Page 2 of 11 http://www.eurjmedres.com/content/19/1/44 infarction in the middle cerebral artery (MCA) territory, attenuated inversion recovery (T1-FLAIR) and T2- neuronal and/or axonal degeneration, loss, dysfunction weighted images. Patients with ILA, significant cerebral and gliosis have been found in the ipsilateral thalamus, atrophy, unstable vital signs or a history of central nervous substantia nigra, and distal pyramidal tract, all of which system disorders were excluded. Demographic character- were remote from the MCA territory [7-12]. The corona istics and vascular risk factors were recorded in each radiata is the core of the hemispheric white matter, and its patient. All patients were investigated with conventional infarction may compromise the integrity of the frontal- MRI, DTI and executive functional assessments at 1 week subcortical white matter connections. A study of patients (6.3 ± 1.1 days, W1), 4 weeks (30.1 ± 2.8 days, W4), and with stroke scanned by traditional magnetic resonance im- 12 weeks (92.8 ± 5.8 days, W12) following a pre-defined aging (MRI) showed that ischemic infarctive lesions affect- protocol. Infarct volume was estimated from the T2- ing the left-sided anterior corona radiata caused executive weighted FLAIR images at W12. For every patient, we dysfunction [4]. The disruption of frontal-subcortical cir- looked for a control of the similar age (±3 years) and cuitry was considered to be responsible for this executive educational history (±2 years) with no current or previous dysfunction. However, whether the left-sided posterior neurological or psychiatric disease. Twelve controls were corona radiata infarction could cause executive dysfunc- recruited over the same period and examined once by tion is unclear. Moreover, the underlying pathogenesis, DTI and an executive functional assessment. especially whether secondary damage in other areas, such as frontal white matter in frontal-subcortical circuitry, due MRI protocol to anterograde and/or retrograde degeneration following MRIs were performed using a 1.5-tesla MRI system focal corona radiata infarction, is a causal phenomenon (Signa General Electric Medical Systems, Milwaukee, and is involved in the dysfunction, is still uncertain. WI, USA) equipped with gradient hardware allowing up The recent development of diffusion tensor imaging to 23 mT/m. T1-FLAIR, fast spin echo T2-weighted im- (DTI), an MRI technique, has shown promise for detect- aging, traditional FLAIR and DTI were performed. Typical ing microstructural changes which are not identified by acquisition parameters of conventional MRI were: T1- traditional MRI. For example, progressive decreased frac- FLAIR (6 mm thick, 2 mm gap, TR 1,475 ms/TE 21.3 ms/ tional anisotropy (FA) values in the pyramidal tract, prox- TI 750.0 ms), T2-FLAIR (3 mm thick, 0 mm gap, TR imal and distal to a subcortical cerebral infarct or pontine 8,000 ms/TE 120.0 ms/TI 2,200 ms). DTI was obtained infarct over 1 to 12 weeks, were found; this means import- with an echo planar imaging (EPI) sequence (3 mm thick, ant loss of structural components in the pyramidal tract 0 mm gap, TR 10,000/TE 100 ms, NEX = 1, matrix 128 × above and below the primary infarcts [11,12]. In patients 128, field of view 24 × 24 cm). DTI was acquired with a b with ischemic leukoaraiosis (ILA), increased mean diffu- factor of 1,000 s/mm2 and diffusion-sensitive gradients sivity (MD) and decreased FA were observed in the frontal were applied along 15 gradient directions. In addition, a and occipital white matter which illustrated axonal loss in reference image without diffusion weighting (b = 0 s/mm2) the regions [6]. These studies suggest potential secondary was acquired. Fifteen repeats were acquired and averaged damage in white matter might be observed by DTI after to improve signal to noise ratio. The scanning baseline corona radiata infarction. was parallel to the antero-posterior commissural (AC-PC) In this study we tested the hypothesis that there is line. Axial slices were obtained using a fast spin echo T2 axonal loss in the left-sided frontal white matter in pa- (3 mm thick, 0 mm gap, TR 5,660 ms/TE 107.7 ms). tients following acute ipsilateral posterior corona radiata infarction as revealed by DTI. We also examined corre- Image post-processing lations of the DTI parameters with executive function in An experienced radiographer carried out image post- these patients. processing without knowing the purpose of the study. The DTI data were transferred to a workstation and spatially Methods filtered using a median 3 × 3 filter. Acquiring the DTI data Participants with the dual-echo EPI sequence and ramp sampling con- The research protocol was approved by the Medical Ethical siderably reduced, but did not eliminate, the geometric Committee of the First Affiliated Hospital, Sun Yat-Sen distortions. We corrected the residual distortions by reg- University, and informed consent was obtained from all istering the diffusion-weighted imaging with the refer- participants. We selected 12 consecutive patients (7 male, ence image using the two-dimensional module of the 5 female) between October 2008 and May 2013 in the automated image registration package (eight-parameter Department of Neurology and Stroke Center, the First with perspective) [13]. With this correction, the DTI pa- Affiliated Hospital, Sun Yat-Sen University, within 7 days rameters were calculated on a pixel-by-pixel basis. Using of a focal infarct in the