International Journal of Neuroscience

ISSN: 0020-7454 (Print) 1543-5245 (Online) Journal homepage: http://www.tandfonline.com/loi/ines20

Injury of the corticobulbar tract in patients with dysarthria following cerebral infarct: diffusion tensor tractography study Hyeok Gyu Kwon, Jun Lee & Sung Ho Jang To cite this article: Hyeok Gyu Kwon, Jun Lee & Sung Ho Jang (2015): Injury of the corticobulbar tract in patients with dysarthria following cerebral infarct: diffusion tensor tractography study, International Journal of Neuroscience, DOI: 10.3109/00207454.2015.1020536 To link to this article: http://dx.doi.org/10.3109/00207454.2015.1020536

Accepted online: 22 May 2015.Published online: 28 Jul 2015.

Submit your article to this journal

Article views: 31

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ines20 Download by: [McMaster University]

Date: 13 October 2015, At: 17:42

International Journal of Neuroscience, 2015; Early Online: 1–5 Copyright © 2015 Taylor and Francis ISSN: 0020-7454 print / 1543-5245 online DOI: 10.3109/00207454.2015.1020536

ORIGINAL ARTICLE

Injury of the corticobulbar tract in patients with dysarthria following cerebral infarct: diffusion tensor tractography study Hyeok Gyu Kwon,1 Jun Lee,2 and Sung Ho Jang1 Department of Physical Medicine and Rehabilitation; 2 Department of Neurology, College of Medicine, Yeungnam University, Daegu, Republic of Korea

Downloaded by [McMaster University] at 17:42 13 October 2015

1

Objectives: Little is known about injury of the corticobulbar tract (CBT) in stroke patients. We attempted to investigate injury of the CBT in patients with dysarthria following cerebral infarct, using diffusion tensor tractography (DTT). Methods: Eight patients with dysarthria following a corona radiata infarct and 12 control subjects were recruited for this study. Diffusion tensor imaging was performed at 14.3 days after onset and reconstruction of the CBT was performed using the probabilistic tractography method. Fractional anisotropy, mean diffusivity, and tract volume of the CBT were measured. Results: Reconstructed CBTs in the affected hemisphere of the patient group were thinner than those of the unaffected hemisphere of the patient group and the control group. Regarding the DTT parameters of the CBTs, fractional anisotropy and tract volume were significantly lower in the affected hemisphere of the patient group than in the unaffected hemisphere of the patient group and the control group (p < 0.05). However, we did not observe any difference in the mean diffusivity value (p > 0.05). Conclusions: We demonstrated injury of the CBT in patients with dysarthria following cerebral infarct in the corona radiata using DTT. This result indicates the importance of CBT evaluation for dysarthria in patients with cerebral infarct. Therefore, we suggest that evaluations of the CBT using DTT would be useful for patients with dysarthria following cerebral infarct. KEYWORDS: diffusion tensor imaging, corticobulbar tract, dysarthria, cerebral infarct

Introduction The corticobulbar tract (CBT), a motor pathway connecting the cerebral cortex to the brainstem, is involved in motor function of the non-oculomotor cranial nuclei [1]. The CBT is composed of the upper motor neurons of the cranial nerves, except for the cranial nerves for oculomotor function. The CBT innervates the nuclei for cranial nerves V, VII, XI, and XII, and also contributes to the cranial nerves IX and X [1]. As a result, the muscles of the face, head, and neck are controlled by the CBT and injury of the CBT can accom-

Received 3 December 2014; revised 14 February 2015; accepted 15 February 2015. Correspondence: Sung Ho Jang, MD, Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, 317-1, Daemyungdong, Namku, Daegu 705-717, Republic of Korea. Tel: +82-53-620-3269. Fax: +82-53-620-3269. E-mail: [email protected]

pany bulbar symptoms such as dysarthria, dysphasia, and facial palsy [1]. Therefore, elucidation of the state of the CBT is needed in order to determine the cause and prognosis for stroke patients with these clinical manifestations. Advances in diffusion tensor tractography (DTT), derived from diffusion tensor imaging (DTI), have enabled three-dimensional reconstruction and estimation of neural tracts for motor function, including the corticospinal tract, corticoreticular pathway, and rubrospinal tract [2–5]. Recent studies have reported on a method for identification and reconstruction of the CBT in the human brain, using DTT [6–8]. In addition, some studies have attempted to apply this technique in patients with brain injury, such as traumatic brain injury and stroke [7,8]. However, little is known about injury of the CBT in stroke patients. In this study, using DTT, we attempted to investigate injury of the CBT in patients with dysarthria following cerebral infarct.

1

Downloaded by [McMaster University] at 17:42 13 October 2015

2

H. G. Kwon et al.

Methods

Table 1. Demographic and clinical data for the patient and control groups.

Subjects

Variables

Eight patients (male: 4, female: 4, mean age: 64.1 ± 10.5 years, range: 49–72 years) and 12 normal healthy control subjects (male: 5, female: 7, mean age: 56.2 ± 8.5 years, range: 47–74 years) with no previous history of neurological, physical, or psychiatric illness were recruited for this study. Inclusion criteria for patients were as follows: (1) first ever stroke, (2) an infarct located in the corona radiata, as confirmed by a neuroradiologist, (3) DTI scanning was performed at an early stage (between 1 and 6 weeks) after onset, (4) dysarthria as defined by the National Institutes of Health Stroke Scale (NIHSS) [9], (5) motor deficits as defined by motricity index (full mark: 100 points), and (6) no apraxia of speech or severe cognitive problems (Mini-Mental State Examination < 25). This study was conducted retrospectively and the study protocol was approved by the Institutional Review Board of our hospital.

Diffusion tensor tractography DTIs were scanned at mean 14.3 days (range: 1–6 weeks) using a six-channel head coil on a 1.5T Philips Gyroscan Intera (Philips, Ltd., Best, The Netherlands) with single-shot echo-planar imaging. For each of the 32 non-collinear diffusion sensitizing gradients, we acquired 67 contiguous slices parallel to the anterior commissure–posterior commissure line. Imaging parameters of DTI were as follows: acquisition matrix = 96 × 96; reconstructed to matrix = 192 × 192; field of view = 240 × 240 mm2 ; repetition time (TR) = 10,398 ms; echo time (TE) = 72 ms; parallel imaging reduction factor (SENSE factor) = 2; echo-planar imaging (EPI) factor = 59; b = 1000 s/mm2 ; number of excitations (NEX) = 1; and a slice thickness of 2.5 mm. Affine multi-scale two-dimensional registration at the Oxford Centre for Functional Magnetic Resonance Imaging of Brain (FMRIB) Software Library (FSL; www.fmrib.ox.ac.uk/fsl) was used for removal of eddy current-induced image distortions [10]. Fiber tracking was performed using a probabilistic tractography method based on a multi-fiber model, and applied in the current study utilizing tractography routines implemented in FMRIB diffusion [5000 streamline samples, 0.5 mm step lengths, curvature thresholds = 0.2 (corresponding to a minimum angle of approximately ±80 degrees)] [10–12]. CBTs were determined by selection of fibers passing through two regions of interest (ROIs). The seed ROI was drawn at the lower portion of the precentral gyrus on the axial image in which the top of the lateral ventricle could be seen [6,7]. The target ROI was given at the portion of

Sex (male:female) Mean age (year) Lesion side (right:left) NIHSS Motricity index Mean days to DTT or duration from onset (days)

Patient group Control group 4:4 64.1 (10.5) 3:5 7.4 (1.7) 43.0 14.3 (10.7)

5:7 56.2 (8.5)

Values represent mean (±standard deviation). NIHSS: National Institutes of Health Stroke Scale; DTT: diffusion tensor tractography.

the CBT area (between transverse pontine fibers and the middle cerebellar peduncle) at the level of mid pons with the axial image [6,7]. Out of 5000 samples generated from each seed voxel, results for each connection were visualized at a threshold of non-zero streamline through each voxel for analysis. We measured values of fractional anisotropy (FA), mean diffusivity (MD), and tract volume of the CBT using MATLABTM (Matlab R2007b, The Mathworks, Natick, MA, USA).

Statistical analysis SPSS software (v.15.0; SPSS, Chicago, IL) was used for data analysis. An independent t-test was used for determination of differences in DTT parameters of the CBTs between the patient group and the control group, and between the affected and unaffected hemispheres in the patient group. The significant level of the p value was set at 0.05.

Results A summary of the demographic data for the patient and control group is shown in Table 1. Reconstructed CBTs in the affected hemisphere of the patient group were thinner than those of the unaffected hemisphere of the patient group and the control group (Figure 1). Regarding the DTT parameters of the CBTs, the FA and tract volume were significantly lower in the affected hemisphere of the patient group than in the unaffected hemisphere of the patient group and the control group (p < 0.05) (Table 2). However, no significant difference was observed in the MD value (p > 0.05). By contrast, no significant differences in the FA, MD, and tract volume were observed between the unaffected hemisphere of the patient group and the control group, and between the right and left hemispheres in the control group (p > 0.05). International Journal of Neuroscience

3

Downloaded by [McMaster University] at 17:42 13 October 2015

Injury of the corticobulbar tract

Figure 1. Brain MR images and results of diffusion tensor tractography for the corticobulbar tract

(CBT). (A) T2-weighted brain MR image shows an infarct in the left corona radiata (72-year-old female patient). (B) CBTs are reconstructed in both hemispheres. The CBT (red) in the affected hemisphere is thinner compared with that of the unaffected hemisphere (green). (C) CBTs (right: green; left: red) are reconstructed in both hemispheres of control subjects.

Discussion In the current study, we recruited eight patients with dysarthria following a cerebral infarct in the corona radiata; our results were as follows: lower FA value and tract volume of the CBT were observed in the affected  C

2015 Taylor and Francis

hemisphere of the patient group than in the unaffected hemisphere of the patient group and the control group, without significant change in the MD value. The FA value represents the white matter organization: in detail, the degree of directionality and integrity of white matter microstructures, such as axons, myelin, and

4

H. G. Kwon et al. Table 2. Diffusion tensor tractography parameters of the corticobulbar tract in the patient and control groups. Hemisphere

FA

MD

Tract volume

Patient group

Affected Unaffected

0.44a (0.02) 0.48 (0.04)

0.78 (0.06) 0.82 (0.03)

180.9a (149.6) 737.5 (190.91)

Control group

Both

0.49 (0.02)

0.79 (0.03)

857.5 (247.3)

Downloaded by [McMaster University] at 17:42 13 October 2015

Values represent mean (±standard deviation). FA: fractional anisotropy; MD: mean diffusivity. a Significant differences between the affected and unaffected hemisphere in the patient group and between the affected hemisphere of the patient group and both hemispheres of the control group, p < 0.05.

microtubules; in contrast, the MD value indicates the magnitude of water diffusion [13,14]. The tract volume is determined by counting the number of voxels contained within a neural tract [15]. Therefore, the decrement of FA value and tract volume without a change in the MD value of the CBT in the affected hemisphere of the patient group indicates injury of the CBT [14,15]. Based on our results, DTT findings of the injured CBTs in our patients provided objective evidence of dysarthria; therefore, the dysarthria in our patients appeared to be attributed to injury of the CBT in the affected hemisphere. Our results suggest the necessity of evaluation of the CBT using DTT for patients who show dysarthria following cerebral infarct. Since introduction of DTI, several studies have reported on the CBT in the human brain [6–8,16,17]. However, among these studies, we believe that only a few studies have provided a precise reconstruction of the CBT [6–8]. In 2012, Pan et al. investigated the somatotopic location of motor pathways in the posterior limb of the internal capsule [6]. They found that the somatotopic fibers were located with anteroposterior alignment (tongue, face, hand, foot) in the posterior limb of the internal capsule. In 2013, Liegeois et al. reconstructed the dorsal and ventral CBTs for lips/larynx and tongue representation, respectively, in 17 children with dysarthria following traumatic brain injury [7]. They found that the left dorsal CBT was critical to the normal execution of speech. During the same year, Yim et al. attempted to localize the CBT in the internal capsule by analyzing the relation between bulbar symptom and lesion location of a cerebral infarct [8]. They reported that the CBT is located beyond the midpoint of the posterior limb of the internal capsule. By contrast, in the current study, we demonstrated injury of the CBT in the corona radiata in stroke patients with dysarthria. Limitations of this study should be considered. First, the study included a relatively small number of subjects. This study was conducted retrospectively; therefore, conduct of further prospective studies including larger numbers of subjects should be encouraged. Second, the wide range of DTI scanning time (1–6 weeks) after onset might be a limi-

tation of this study because inflammation and edema in the early stage of cerebral infarct could affect the values of DTT parameters [18], Third, DTI may underestimate or overestimate the fiber tracts due to the fact that regions of fiber complexity and crossing can prevent full reflection of the underlying fiber architecture by DTI [19]. In summary, using DTT, we demonstrated injury of the CBT in patients with dysarthria following cerebral infarct in the corona radiata. This result indicates the importance of evaluation of the CBT for dysarthria in patients with cerebral infarct. Therefore, we suggest that evaluation of the CBT using DTT would be useful for patients with dysarthria following cerebral infarct.

Declaration of Interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. This work was supported by the DGIST R&D Program of the Ministry of Science, ICT and Future Planning (15-BD-0401).

References 1. Afifi AK, Bergman RA. Functional neuroanatomy: text and atlas. 2nd ed. New York: Lange Medical Books/McGraw-Hill; 2005. ix, 494 p. 2. Kunimatsu A, Aoki S, Masutani Y, et al. The optimal trackability threshold of fractional anisotropy for diffusion tensor tractography of the corticospinal tract. Magn Reson Med Sci 2004;3:11–17. 3. Yang HS, Kwon HG, Hong JH, et al. The rubrospinal tract in the human brain: diffusion tensor imaging study. Neurosci Lett 2011;504:45–8. 4. Jang SH, Chang CH, Lee J, et al. Functional role of the corticoreticular pathway in chronic stroke patients. Stroke 2013;44:1099–104. 5. Holodny AI, Gor DM, Watts R, et al. Diffusion-tensor MR tractography of somatotopic organization of corticospinal tracts in the internal capsule: initial anatomic results in contradistinction to prior reports. Radiology 2005;234:649–53. 6. Pan C, Peck KK, Young RJ, Holodny AI. Somatotopic organization of motor pathways in the internal capsule: a proba-

International Journal of Neuroscience

Injury of the corticobulbar tract

7.

8. 9.

10.

11.

Downloaded by [McMaster University] at 17:42 13 October 2015

12.

bilistic diffusion tractography study. AJNR Am J Neuroradiol 2012;33:1274–80. Liegeois F, Tournier JD, Pigdon L, et al. Corticobulbar tract changes as predictors of dysarthria in childhood brain injury. Neurology 2013;80:926–32. Yim SH, Kim JH, Han ZA, et al. Distribution of the corticobulbar tract in the internal capsule. J Neurol Sci 2013;334:63–8. Brott T, Marler JR, Olinger CP, et al. Measurements of acute cerebral infarction: lesion size by computed tomography. Stroke 1989;20:871–5. Smith SM, Jenkinson M, Woolrich MW, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004;23(Suppl. 1):S208–219. Behrens TE, Berg HJ, Jbabdi S, et al. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 2007;34:144–55. Behrens TE, Johansen-Berg H, Woolrich MW, et al. Noninvasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 2003;6:750–7.

 C

2015 Taylor and Francis

5

13. Mori S, van Zijl PC. Fiber tracking: principles and strategies – a technical review. NMR Biomed 2002;15:468–80. 14. Assaf Y, Pasternak O. Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 2008;34:51–61. 15. Seo JP, Jang SH. Different characteristics of the corticospinal tract according to the cerebral origin: DTI study. AJNR Am J Neuroradiol 2013;34:1359–63. 16. Hagmann P, Thiran JP, Jonasson L, et al. DTI mapping of human brain connectivity: statistical fibre tracking and virtual dissection. Neuroimage 2003;19:545–54. 17. Thomas B, Eyssen M, Peeters R, et al. Quantitative diffusion tensor imaging in cerebral palsy due to periventricular white matter injury. Brain 2005;128:2562–77. 18. Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics 2007;4:316–329. 19. Yamada K, Sakai K, Akazawa K, et al. MR tractography: a review of its clinical applications. Magn Reson Med Sci 2009;8:165–74.

Injury of the corticobulbar tract in patients with dysarthria following cerebral infarct: diffusion tensor tractography study.

Little is known about injury of the corticobulbar tract (CBT) in stroke patients. We attempted to investigate injury of the CBT in patients with dysar...
600KB Sizes 1 Downloads 18 Views