Somatosensory & M otor Research
http://informahealthcare.com/smr ISSN: 0899-0220 (print), 1369-1651 (electronic)
informa
Somatosens M o t Res, 2015; 32(1): 2 5 -3 0
healthcare
© 2015 Inform a UK Ltd. DOI: 10.3109/08990220.2014.949006
O RIG INAL ARTICLE
Change of the anterior corticospinal tract on the normal side of the brain in chronic stroke patients: Diffusion tensor imaging study Sung Ho Jang & Hyeok Gyu Kwon Departm ent o f Physical Medicine an d Rehabilitation, College o f Medicine, Yeungnam University, Daegu, Republic o f Korea
A b s tr a c t
K e yw o rd s
We investigated change of the anterior corticospinal tract (CST) on the normal side o f the brain in stroke patients, using diffusion tensor tractography (DTT). We recruited 32 stroke patients and 24 control subjects. Motricity Index and DTT for the whole and anterior CSTs were evaluated. According to findings, the fiber number o f the anterior CST on the normal side o f the brain o f stroke patients was related to poor motor function o f the affected extremities.
Anterior corticospinal tract, diffusion tensor imaging, hemiparesis, motor function, stroke H is t o r y
Received 31 March 2014 Revised 1 June 2014 Accepted 17 July 2014 Published online 28 August 2014
In tro d u c tio n
The corticospinal tract (CST) is a major neural tract for motor function in the human brain. Three separate CSTs are known to exist in the human brain; the crossed lateral CST, the uncrossed lateral CST, and the uncrossed anterior (ventral) CST (Nyberg-Hansen and Rinvik 1963; York 1987; Davidoff 1990; Nathan et al. 1990; Canedo 1997). However, the CST is generally divided into the crossed lateral CST and the uncrossed anterior CST. The lateral CST is formed by decussation of 75-90% of CST fibers at the medulla; in contrast, the anterior CST, which does not cross the medulla, occupies 5-15% of the entire CST (Nyberg-Hansen and Rinvik 1963; Davidoff 1990). Many previous studies have reported involvement of the lateral CST in motor function of distal muscles, especially finger extensors (York 1987; Davidoff 1990; Mendoza and Foundas 2007; Cho et al. 2012). However, the function of the anterior CST has not been clearly elucidated. The anterior CST has been reported to primarily innervate the proximal muscles, such as the musculature of the neck, trunk, and proximal upper extremities (Nyberg-Hansen and Rinvik 1963; Davidoff 1990; Canedo 1997). On the other hand, the anterior CST has been suggested as one of the ipsilateral motor pathways from the unaffected motor cortex to the affected hand, which contribute to motor recovery following stroke (Turton et al. 1996; Netz et al. 1997; Kim et al. 2004; Jang 2009a).
Correspondence: Hyeok Gyu Kwon, Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, 317-1, Daemyung dong, Namku, Daegu 705-717, Republic of Korea. Tel: +82 53 620 4098. Fax: +82 53 625 3508. E-mail: [email protected]
These ipsilateral motor pathways have been demonstrated using various brain mapping techniques, including functional magnetic resonance imaging (MRI), transcranial magnetic stimulation, and diffusion tensor imaging (DTI) (Chollet et al. 1991; Turton et al. 1996; Cicinelli et al. 1997; Netz et al. 1997; Terakawa et al. 2000; Ago et al. 2003; Kim et al. 2004; Jang 2009a). However, little is known about the role of the anterior CST in stroke patients. The main reason for lack of research on the anterior CST in stroke patients was that a specific method for evaluation of the anterior CST has not been available for use in the live human brain. Diffusion tensor tractography (DTT) derived from DTI, which can detect water diffusion in a preferential direction, enables investigation of the CST in the live human brain (Mori et al. 1999). Therefore, many studies of the CST in the human brain have been reported (Mori et al. 1999; Guye et al. 2003; Wakana et al. 2004; Lee et al. 2005). In addition, it also enables acquisition of quantitative data on the neural structure, including the fractional anisotropy (FA), which represents the white matter organization, and is influenced by axonal myelination, density, and the degree of directionality; the apparent diffusion coefficient (ADC) indicates the magnitude of water diffusion; and the fiber number (FN) which reflects the total number of voxels in a neural tract (Alexander et al. 2007; Assaf and Pasternak 2008; Neil 2008). A recent study using DTT reported on a method for three-dimensional identification of the anterior CST (Kwon et al. 2011). In the current study, using DTT, we attempted to investigate change of the anterior CST in terms of the FA, ADC, and FN on the normal side of the brain in order to determine whether it contributes to motor function in chronic hemiplegic stroke patients.
26
S. H. Jang & H. G. Kwon
Somatosens Mot Res, 2015; 32(1): 25-30
M e th o d s Subjects
Thirty-two patients (males: 17, females: 15, mean age: 56.3 years, range: 27-79 years) and 24 age- and sex-matched control subjects (males: 13, females: 11, mean age: 44.6 years, range: 21-77 years) with no previous history of psychiatric, neuro logical, or physical illness were recruited for this study. Inclusion criteria for patients were as follows: (1) first ever stroke, (2) more than 3 months after stroke onset, (3) definite motor weakness in the affected extremities at the time of DTI scanning: below grade 4 on the Medical Research Council Scale in any key muscle of extremities, and (4) patients with apraxia or severe cognitive problems (Mini-Mental State Examination 0.2 and ended al a voxel with FA < 0.2 and a tract turning angle 0.05). However, the FN of the anterior CST on the normal side of the brain for the patient group showed moderate negative correlation with upper MI ( r = —0.57, p = 0.001) and total MI ( r = —0.44, /? = 0.011), but did not show correlation with lower MI ( r = —0.24, p = 0.189) (Figure 2) (Rea and Parker 2005).
significantly lower than those of both sides of the brain for the control group (p< 0.05). By contrast, the ADC value of the whole CST on the normal side of the brain for the patient group was higher than that of both sides of the brain for the control group, without significant difference in the anterior CST (/?< 0.05, >0.05, respectively). Regarding the FN, the normal side of the brain for the patient group showed a higher value than both sides of the brain for the control group in the anterior CST ( p < 0.05), however, no significant difference was observed in the whole CST (p> 0.05). Table IV shows the correlations between MI and DTT parameters of the whole and anterior CSTs on the normal side of the brain for the patient group (Table IV). In terms of the FA, ADC, and FN of the whole CST on the normal side of the brain for the patient group, we found no significant correl ation with all Mis (/? > 0.05). Likewise, the FA and ADC of the anterior CST on the normal side of the brain for the
D is c u s s io n
In the current study, using DTT, we investigated change of the anterior CST on the normal side of the brain in chronic hemiparetic stroke patients. In addition, we attempted to elucidate its association with motor weakness in the affected extremities and observed the following results: (1) the FA values of the whole and anterior CSTs in the patient group
MI
Table II. Demographic and clinical data according to diffusion tensor tractography type for the patient and control groups. Variables Sex (male:female) Mean age, years Stroke type (infarct:hemorrhage) Lesion side (rightdeft) Lesion location Infarction (ACA, MCA, PCA, Mid) Hemorrhage (cortex, BG, thalamus) Motricity Index Mean month to DTT or duration front onset, months
Patient group
Control group
17:15 56.3 (15.2) 20:12 11:21
13:11 44.6 (14.9)
U pper M I
90
(Upper M 0
80
♦
♦
♦
♦♦
70 60 50 40 -
♦ ♦
20
2:16:0:2 2:6:4 46.9 (22.9) 7.9 (3.6)
‘ " r * = - 0 .5 7
10
♦ # 0
Values represent mean ( ± standard deviation), ACA: anterior cerebral artery, MCA: middle cerebral artery, PCA: posterior cerebral artery. Mid: midbrain, BG: basal ganglia, DTT: diffusion tensor tractography.
100
200
500
300
T * -600
F ib e r 700 n u m b e r
Figure 2. Correlation between upper Motricity Index and fiber number of the anterior corticospinal tract on the normal side of the brain for the patient group. *p< 0.05.
Table III. Diffusion tensor tractography parameters for the whole and anterior corticospinal tract on the normal side of the brain for the patient group and average of both sides of the brain for the control group. CST
Group
Whole
Patient Control Patient Control
Anterior
FA 0.55 0.58 0.53 0.56
(0.02) (0.02) (0.03) (0.03)
ADC
p Value 0.000* 0.000*
0.87 0.82 0.93 0.91
(0.07) (0.04) (0.1) (0.07)
p Value
p Value
FN
0.000*
1657.2 (695.2) 1533.7 (328.8) 299.7 (147.5) 194.56 (74.5)
0.22
0.29 0.000*
Values represent mean (± standard deviation), CST: corticospinal tract, FA: fractional anisotropy, ADC: apparent diffusion coefficients (x 10_3mm2/s), FN: fiber number. *p
http://informahealthcare.com/smr ISSN: 0899-0220 (print), 1369-1651 (electronic)
informa
Somatosens M o t Res, 2015; 32(1): 2 5 -3 0
healthcare
© 2015 Inform a UK Ltd. DOI: 10.3109/08990220.2014.949006
O RIG INAL ARTICLE
Change of the anterior corticospinal tract on the normal side of the brain in chronic stroke patients: Diffusion tensor imaging study Sung Ho Jang & Hyeok Gyu Kwon Departm ent o f Physical Medicine an d Rehabilitation, College o f Medicine, Yeungnam University, Daegu, Republic o f Korea
A b s tr a c t
K e yw o rd s
We investigated change of the anterior corticospinal tract (CST) on the normal side o f the brain in stroke patients, using diffusion tensor tractography (DTT). We recruited 32 stroke patients and 24 control subjects. Motricity Index and DTT for the whole and anterior CSTs were evaluated. According to findings, the fiber number o f the anterior CST on the normal side o f the brain o f stroke patients was related to poor motor function o f the affected extremities.
Anterior corticospinal tract, diffusion tensor imaging, hemiparesis, motor function, stroke H is t o r y
Received 31 March 2014 Revised 1 June 2014 Accepted 17 July 2014 Published online 28 August 2014
In tro d u c tio n
The corticospinal tract (CST) is a major neural tract for motor function in the human brain. Three separate CSTs are known to exist in the human brain; the crossed lateral CST, the uncrossed lateral CST, and the uncrossed anterior (ventral) CST (Nyberg-Hansen and Rinvik 1963; York 1987; Davidoff 1990; Nathan et al. 1990; Canedo 1997). However, the CST is generally divided into the crossed lateral CST and the uncrossed anterior CST. The lateral CST is formed by decussation of 75-90% of CST fibers at the medulla; in contrast, the anterior CST, which does not cross the medulla, occupies 5-15% of the entire CST (Nyberg-Hansen and Rinvik 1963; Davidoff 1990). Many previous studies have reported involvement of the lateral CST in motor function of distal muscles, especially finger extensors (York 1987; Davidoff 1990; Mendoza and Foundas 2007; Cho et al. 2012). However, the function of the anterior CST has not been clearly elucidated. The anterior CST has been reported to primarily innervate the proximal muscles, such as the musculature of the neck, trunk, and proximal upper extremities (Nyberg-Hansen and Rinvik 1963; Davidoff 1990; Canedo 1997). On the other hand, the anterior CST has been suggested as one of the ipsilateral motor pathways from the unaffected motor cortex to the affected hand, which contribute to motor recovery following stroke (Turton et al. 1996; Netz et al. 1997; Kim et al. 2004; Jang 2009a).
Correspondence: Hyeok Gyu Kwon, Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University, 317-1, Daemyung dong, Namku, Daegu 705-717, Republic of Korea. Tel: +82 53 620 4098. Fax: +82 53 625 3508. E-mail: [email protected]
These ipsilateral motor pathways have been demonstrated using various brain mapping techniques, including functional magnetic resonance imaging (MRI), transcranial magnetic stimulation, and diffusion tensor imaging (DTI) (Chollet et al. 1991; Turton et al. 1996; Cicinelli et al. 1997; Netz et al. 1997; Terakawa et al. 2000; Ago et al. 2003; Kim et al. 2004; Jang 2009a). However, little is known about the role of the anterior CST in stroke patients. The main reason for lack of research on the anterior CST in stroke patients was that a specific method for evaluation of the anterior CST has not been available for use in the live human brain. Diffusion tensor tractography (DTT) derived from DTI, which can detect water diffusion in a preferential direction, enables investigation of the CST in the live human brain (Mori et al. 1999). Therefore, many studies of the CST in the human brain have been reported (Mori et al. 1999; Guye et al. 2003; Wakana et al. 2004; Lee et al. 2005). In addition, it also enables acquisition of quantitative data on the neural structure, including the fractional anisotropy (FA), which represents the white matter organization, and is influenced by axonal myelination, density, and the degree of directionality; the apparent diffusion coefficient (ADC) indicates the magnitude of water diffusion; and the fiber number (FN) which reflects the total number of voxels in a neural tract (Alexander et al. 2007; Assaf and Pasternak 2008; Neil 2008). A recent study using DTT reported on a method for three-dimensional identification of the anterior CST (Kwon et al. 2011). In the current study, using DTT, we attempted to investigate change of the anterior CST in terms of the FA, ADC, and FN on the normal side of the brain in order to determine whether it contributes to motor function in chronic hemiplegic stroke patients.
26
S. H. Jang & H. G. Kwon
Somatosens Mot Res, 2015; 32(1): 25-30
M e th o d s Subjects
Thirty-two patients (males: 17, females: 15, mean age: 56.3 years, range: 27-79 years) and 24 age- and sex-matched control subjects (males: 13, females: 11, mean age: 44.6 years, range: 21-77 years) with no previous history of psychiatric, neuro logical, or physical illness were recruited for this study. Inclusion criteria for patients were as follows: (1) first ever stroke, (2) more than 3 months after stroke onset, (3) definite motor weakness in the affected extremities at the time of DTI scanning: below grade 4 on the Medical Research Council Scale in any key muscle of extremities, and (4) patients with apraxia or severe cognitive problems (Mini-Mental State Examination 0.2 and ended al a voxel with FA < 0.2 and a tract turning angle 0.05). However, the FN of the anterior CST on the normal side of the brain for the patient group showed moderate negative correlation with upper MI ( r = —0.57, p = 0.001) and total MI ( r = —0.44, /? = 0.011), but did not show correlation with lower MI ( r = —0.24, p = 0.189) (Figure 2) (Rea and Parker 2005).
significantly lower than those of both sides of the brain for the control group (p< 0.05). By contrast, the ADC value of the whole CST on the normal side of the brain for the patient group was higher than that of both sides of the brain for the control group, without significant difference in the anterior CST (/?< 0.05, >0.05, respectively). Regarding the FN, the normal side of the brain for the patient group showed a higher value than both sides of the brain for the control group in the anterior CST ( p < 0.05), however, no significant difference was observed in the whole CST (p> 0.05). Table IV shows the correlations between MI and DTT parameters of the whole and anterior CSTs on the normal side of the brain for the patient group (Table IV). In terms of the FA, ADC, and FN of the whole CST on the normal side of the brain for the patient group, we found no significant correl ation with all Mis (/? > 0.05). Likewise, the FA and ADC of the anterior CST on the normal side of the brain for the
D is c u s s io n
In the current study, using DTT, we investigated change of the anterior CST on the normal side of the brain in chronic hemiparetic stroke patients. In addition, we attempted to elucidate its association with motor weakness in the affected extremities and observed the following results: (1) the FA values of the whole and anterior CSTs in the patient group
MI
Table II. Demographic and clinical data according to diffusion tensor tractography type for the patient and control groups. Variables Sex (male:female) Mean age, years Stroke type (infarct:hemorrhage) Lesion side (rightdeft) Lesion location Infarction (ACA, MCA, PCA, Mid) Hemorrhage (cortex, BG, thalamus) Motricity Index Mean month to DTT or duration front onset, months
Patient group
Control group
17:15 56.3 (15.2) 20:12 11:21
13:11 44.6 (14.9)
U pper M I
90
(Upper M 0
80
♦
♦
♦
♦♦
70 60 50 40 -
♦ ♦
20
2:16:0:2 2:6:4 46.9 (22.9) 7.9 (3.6)
‘ " r * = - 0 .5 7
10
♦ # 0
Values represent mean ( ± standard deviation), ACA: anterior cerebral artery, MCA: middle cerebral artery, PCA: posterior cerebral artery. Mid: midbrain, BG: basal ganglia, DTT: diffusion tensor tractography.
100
200
500
300
T * -600
F ib e r 700 n u m b e r
Figure 2. Correlation between upper Motricity Index and fiber number of the anterior corticospinal tract on the normal side of the brain for the patient group. *p< 0.05.
Table III. Diffusion tensor tractography parameters for the whole and anterior corticospinal tract on the normal side of the brain for the patient group and average of both sides of the brain for the control group. CST
Group
Whole
Patient Control Patient Control
Anterior
FA 0.55 0.58 0.53 0.56
(0.02) (0.02) (0.03) (0.03)
ADC
p Value 0.000* 0.000*
0.87 0.82 0.93 0.91
(0.07) (0.04) (0.1) (0.07)
p Value
p Value
FN
0.000*
1657.2 (695.2) 1533.7 (328.8) 299.7 (147.5) 194.56 (74.5)
0.22
0.29 0.000*
Values represent mean (± standard deviation), CST: corticospinal tract, FA: fractional anisotropy, ADC: apparent diffusion coefficients (x 10_3mm2/s), FN: fiber number. *p
