NeuroRehabilitation xx (20xx) x–xx 1

DOI:10.3233/NRE-130945
IOS Press

1 Motor recovery by improvement of

2 limb-kinetic apraxia in a chronic stroke
patient

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4 Sung Ho Jang∗
5 Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University 317-1,

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6 Daemyungdong, Namku, Taegu, 705-717, Republic of Korea. Tel./Fax: +82 53 620 3269;
7 E-mail: strokerehab@hanmail.net.

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8 Abstract.
9 OBJECTIVES: We report on a chronic stroke patient who showed motor recovery by improvement of limb-kinetic apraxia (LKA)
10 after undergoing intensive rehabilitation for a period of one month, which was demonstrated by diffusion tensor tractography
11 (DTT) and transcranial magnetic stimulation (TMS).
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12 METHODS: A 50-year-old male patient presented with severe paralysis of the left extremities at the onset of thalamic hemorrhage.
13 At thirty months after onset, the patient exhibited moderate weakness of his left upper and lower extremities. In addition, he
14 exhibited a slow, clumsy, and mutilated movement pattern during grasp-release movements of his left hand. During a one-month
15 period of intensive rehabilitation, which was started at thrity months after onset, the patient showed 22% motor recovery of the
16 left extremities. The slow, clumsy, and mutilated movement pattern of the left hand almost disappeared.
17 RESULTS: DTTs of the corticospinal tract (CST) in both hemispheres originated from the cerebral cortex, including the primary
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18 motor cortex, and passed along the known CST pathway. The DTT of the right CST was located anterior to the old hemorrhagic
19 lesion. TMS study performed at thirty and thirty-one months after onset showed normal and similar findings for motor evoked
20 potential in terms of latency and amplitude of the left hand muscle.
21 CONCLUSIONS: We think that the motor weakness of the left extremities in this patient was mainly ascribed to LKA and that
22 most of the motor recovery during a one-month period of rehabilitation was attributed to improvement of LKA.
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23 Keywords: Motor recovery, stroke, diffusion tensor tractography, transcranial magnetic stimulation, apraxia, limb-kinetic apraxia
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1. Introduction Apraxia is defined as the inability to perform learned

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24 32

skilled movements in spite of preservation of power, 33

25 Stroke is a leading cause of major disability in sensation, and comprehension for execution of move- 34

26 adults. Motor weakness is one of the most serious ments [9–11]. Limb-kinetic apraxia (LKA), one of 35

27 disabling sequelae of stroke, with more than 50% of the apraxias, is defined as the execution disorder 36

28 stroke patients experiencing a residual motor deficit of movements, resulting from injury of the premo- 37

29 [6]. Injury of neural tracts affecting motor function tor cortex (PMC) or the corticofugal tract from the 38

30 is accompanied by motor weakness, however, apraxia PMC with preservation of the corticospinal tract (CST) 39

31 can also accompany motor weakness like symptoms. [12, 19, 21, 26].

1053-8135/13/$27.50 © 2013 – IOS Press and the authors. All rights reserved
 2 S.H. Jang / Motor recovery by improvement of limb-kinetic apraxia

40 Diagnosis of LKA can be difficult because it is made Table 1

41 by clinical observation of movements with confirmation Changes of motor function and the results of transcranial magnetic
stimulation in the patient
42 of the CST state. Diffusion tensor tractography (DTT),
Duration from onset Onset 30 months 31 months
43 derived from diffusion tensor imaging (DTI), provides
44 a unique advantage for three-dimensional visualization MRC Shoulder abductor 0 3+ 4+
Elbow flexor 0 4 5
45 and estimation of the CST [13, 16, 17, 24]. Transcranial Finger flexor 0 3+ 4+
46 magnetic stimulation (TMS) stimulates the neurons of Finger extensor 0 3 4
the CST and provides a unique advantage for estimating Hip flexor 0 3+ 4+

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Knee extensor 0 4 5
the amount of CST fibers by measuring amplitude of

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Ankle dorsiflexor 0 2+ 4
49 motor evoked potential (MEP) [27]. Therefore, TMS MI Upper extremity 0 65 84
50 could be useful for demonstrating change in the amount Lower extremity 0 57 83
51 of CST fibers. Total 0 61 83
TMS Latency (msec) 22.3 22.7
52 In the current study, we report on a chronic stroke Amplitude (␮V) 4000 4000
patient who showed motor recovery by improvement

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MRC: Medical Research Council, MI: Motricity Index, TMS: Tran-
54 of LKA after undergoing intensive rehabilitation for a scranial magnetic stimulation.
55 period of one month, which was demonstrated by DTT
56 and TMS. sation (20: full mark: 24), he showed mild impairment 88

57 2. Case report
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of somatosensory function [23]. The patient exhibited
moderate weakness of his left upper and lower extrem-
ities (MI: 61) (Table 1). In addition, he exhibited slow,
89

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clumsy, and mutilated movements when performing 92

58 The standardized Motricity Index (MI) and Medical grasp-release movements of his left hand. He walked 93

59 Research Council (MRC) were used for determination with a pattern of spastic circumduction and severe 94

60 of motor function [2, 4]. The MI, with a maximum score associated reaction of the left elbow. T2-weighted MR 95

of 100, is a measure of the integrity of extremity motor images taken at thirty months after onset showed an
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61 96

62 function. Reliability and validity of the MI are well- old hemorrrhagic lesion in the right thalamus, poste- 97

63 established [4]. The MRC score was used for evaluation rior limb of the internal capsule, and midbrain (Fig. 1). 98

64 of motor function: 0, no contraction; 1, palpable con- The patient provided signed, informed consent and our 99

65 traction but no visible movement; 2, movement without institutional review board approved the study protocol. 100

66 gravity; 3, movement against gravity; 4, movement The patient participated in a comprehensive reha- 101
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67 against a resistance lower than the resistance overcome bilitative management program, including movement 102

68 by the healthy side; and 5, movement against a resis- therapy, dopaminergic drugs for improvement of 103

69 tance equal to the maximum resistance overcome by the apraxia (ropinorole, 3 mg; bromocriptine, 10 mg; lev- 104

70 healthy side [2]. odopa, 375 mg), antispastic drugs (baclofen 45 mg), 105

A 50-year-old, right-handed male patient presented and neuromuscular electrical stimulation therapy of the
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71 106

72 with severe paralysis of the left upper and lower extrem- left elbow extensors, finger extensors, knee extensors, 107

73 ities at the onset of thalamic hemorrhage (MI: 0). The and ankle dorsiflexors (two times, 20 minutes/time, 108

74 patient received conservative management at the neu- seven days/week). Movement therapy was performed 109

75 rosurgery department of a university hospital and then primarily for improvement of motor function, move- 110
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76 underwent rehabilitation at a local rehabilitation hospi- ment pattern of the left extremities, and postural control, 111

77 tal. However, he could not perform most daily activities and was performed six days (Monday through Friday: 112

78 using his left hand and could not walk independently 2.5 hours/day, Saturday: one hour/day) per week. Dur- 113

without a cane. At thirty months after stroke onset, the ing a one-month period of intensive rehabilitation, the
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79 114

80 patient was admitted to the rehabilitation department patient showed motor recovery of the left upper and 115

81 of a university hospital in order to undergo intensive lower extremities of as much as 22% on MI (61–>83). 116

82 rehabilitation. At the time of admission, the patient’s In addition, his slow, clumsy, and mutilated movement 117

83 scores on the Mini-Mental State Exam and the ideo- pattern when performing grasp-release movements of 118

84 motor apraxia test were 28 (cut-off score <25) and 40 his left hand almost disappeared. He was able to walk 119

85 (cut-off score <32), respectively [3, 7]. According to independently, showing marked improvement of spas- 120

86 the Nottingham Sensory Assessment (The subscales for tic circumduction gait pattern and severe associated 121

87 tactile sensation (16, full mark: 20) and kinesthetic sen- reaction of the left elbow. 122
 S.H. Jang / Motor recovery by improvement of limb-kinetic apraxia 3

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30-month 1mV 31-month 1mV

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Fig. 1. A. T2-weighted brain MR images show an old hemorrhagic lesion in the right thalamus, posterior limb of the internal capsule, and
midbrain. B. Diffusion tensor tractography for the corticospinal tract of the affected hemisphere at thirty months after onset was similar to that of
the hemisphere of the unaffected side. The old hemorrhagic lesion (arrow) was located posterior to the right corticospinal tract. C. Motor-evoked
potentials obtained from the left abductor pollicis brevis muscle at thirty and thirty-one months after onset showed similar latency and amplitude.
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123 2.1. Diffusion tensor tractography contiguous slices parallel to the anterior commissure- 129

posterior commissure line. Scanning was performed 130

124 A 6-channel head coil on a 1.5 T Philips Gyroscan from the cortex to the middle of the second cer- 131

125 Intera (Philips, Ltd., Best, the Netherlands) with vical vertebral body. Imaging parameters were 132

126 single-shot echo-planar imaging was used for acqui- as follows: acquisition matrix = 96 × 96; recon- 133

127 sition of DTI data. For each of the 32 non-collinear structed to matrix = 192 × 192 matrix; field of view 134

128 diffusion sensitizing gradients, we acquired 70 = 240 mm × 240 mm; TR = 10,398 ms; TE = 72 ms; 135
 4 S.H. Jang / Motor recovery by improvement of limb-kinetic apraxia

136 parallel imaging reduction factor (SENSE factor) = 2; characteristics of LKA are as follows [5, 9, 12, 21, 182

137 EPI factor = 59; b = 1000 s/mm2 ; NEX = 1; and a slice 22]: 1) awkward, clumsy, coarse, mutilated pattern of 183

138 thickness of 2.5 mm (acquired isotropic voxel size execution of simple movements, confined mainly to 184

139 2.5 mm × 2.5 mm × 2.5 mm). The fiber assignment movements of the affected hand, 2) resulting mainly 185

140 continuous tracking (FACT) algorithm implemented from frontal lobe damage centered on the PMC or the 186

141 within the DTI task card software (Philips Extended corticofugal tract from the PMC with preservation of the 187

142 MR WorkSpace 2.6.3) was used in performance of CST, 3) no voluntary-automatic dissociation, 4) differ- 188

fiber tracking [24]. For CST analysis, a seed region of entiation from concurrent limb weakness resulting from

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interest (ROI) was placed on the CST at the anterior injury of the CST is difficult because it is similar to the

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145 pontomedullary junction on an axial slice and a target motor weakness observed following CST injury, and 5) 191

146 ROI was drawn in the CST area of the anterior medulla normal conceptual knowledge of motor performance. 192

147 [14]. The termination criteria applied were fractional In this patient, we observed 22% motor recovery for 193

148 anisotropy (FA) <0.2 and an angle change of >45 a period of one month from thirty months after onset. 194

degrees [17]. We think that the motor weakness of the left extrem-

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149 195

150 Results of DTT of the right and left CST showed that ities in this patient was mainly ascribed to LKA and 196

151 fiber tracts originated from the cerebral cortex, includ- that most of the motor recovery during a one-month 197

152 ing the primary motor cortex, and passed along the period of rehabilitation was attributed to improvement 198

153

154
known CST pathway (Fig. 1-B). DTT of the right CST
was located anterior to the old hemorrhagic lesion. or
of LKA, for the following reasons. First, we con-
firmed that the CST in the affected (right) hemisphere
showed normal findings in terms of MEP parameters
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200

201
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155 2.2. Transcranial Magnetic Stimulation (latency and amplitude) on TMS and configuration 202

on DTT [15]. However, the patient exhibited moder- 203

156 A Magstim Novametrix 200 magnetic stimulator ate motor weakness in the left extremities until thirty 204

157 with a 9-cm mean diameter circular coil (Novametrix months after onset. The clinical characteristics of left 205

Inc.) was used in performance of TMS. Cortical stim- hand movements (slow, clumsy, and mutilated) were
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158 206

159 ulation was performed with the coil held tangentially also compatible with those of LKA. However, because 207

160 over the vertex. Stimulation of the left hemisphere the patient showed normal cognition for motor perfor- 208

161 was provided by a counterclockwise current, and mance and a normal result on the ideomotor apraxia 209

162 stimulation of the right hemisphere was provided by test (20: cut-off score <32), we were able to rule out 210

163 a clockwise current. Four motor-evoked potentials ideational and ideomotor apraxia. Second, the patient 211
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164 (MEPs) were obtained from both abductor pollicis had a lesion around the CST in the posterior limb of 212

165 brevis (APB) muscles in a relaxed state. Stimulation the internal capsule, which is known to related to the 213

166 intensity was set at the maximum stimulator output. corticofugal tract from the PMC, which is responsi- 214

167 Each site was stimulated three times with inter-stimulus ble for LKA [5, 8, 9, 12, 21, 25]. Third, he showed 215

intervals of >10 seconds, and MEP having the shortest rapid motor recovery for one month from thirty months
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168 216

169 latency and the average peak-to-peak amplitudes was after onset, which is well-known as the plateau stage 217

170 adopted. of motor recovery in stroke patients. Considering the 218

171 TMS study performed at thirty and thirty-one months amplitudes of MEP, which indicate that the fiber num- 219

172 after onset showed similar MEP findings at the left bers of the CST in the affected hemisphere were not 220
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173 APB muscle (thirty months: latency- 22.3 msec; ampli- changed between thirty and thirty-one months, we can 221

174 tude: 4000 uV), thirty-one months: latency- 22.7 msec; assume that the motor recovery was mainly attributed 222

175 amplitude: 4000 uV). to improvement of LKA. In particular, dopaminergic 223

drugs, which have been reported to be effective for

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224

treatment of apraxia, appeared to have been effective 225

176 3. Discussion for improvement of LKA [18, 20, 28, 29]. 226

To the best of our knowledge, only a few studies 227

177 Diagnosis of LKA is difficult because there are using DTI have reported on LKA [1, 12]. In 2008, in an 228

178 no specific diagnostic tools; instead, it is dependent investigation of changes in white matter in 21 patients 229

179 on clinical observation of movements. The nature of with corticobasal degeneration syndrome, Borroni et al. 230

180 LKA has not been clearly elucidated, therefore, it has reported correlation of limb apraxia with parietal atro- 231

181 been controversial. Summarizing previous studies, the phy and with FA reductions in parietofrontal associative 232
 S.H. Jang / Motor recovery by improvement of limb-kinetic apraxia 5

233 fibers [1]. In addition, the limb-kinetic component of [7] Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). Mini- 280

234 apraxia showed correlation with reduction of hand mental state. A practical method for grading the cognitive state 281
of patients for the clinician. J Psychiatr Res, 12, 189-198. 282
235 sensorimotor connecting fibers. Recently, Hong et al. [8] Freund, H. J. (1990). Premotor area and preparation of move- 283
236 [2012] reported on a patient with ideomotor apraxia and ment. Rev Neurol (Paris), 146, 543-547. 284

237 LKA following a cerebral infarct in the left frontal cor- [9] Gross, R. G., & Grossman, M. (2008). Update on apraxia. Curr 285

238 tex [12]. They demonstrated the partial injuries of the Neurol Neurosci Rep, 8, 490-496. 286
[10] Heilman, K. M. (2010). Apraxia. Continuum (Minneap Minn), 287
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fasciculus in the affected hemisphere that were respon-

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240 [11] Heilman, K. M., & Valenstein, E., (2003) Clinical neuropsy- 289

sible for LKA and ideomotor apraxia, respectively.

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241 chology, Oxford, New York: Oxford University Press, pp. 15, 290

242 In conclusion, we report on a patient who showed 716. 291

[12] Hong, J. H., Lee, J., Cho, Y. W., Byun, W. M., Cho, H. K., 292
243 motor recovery during a one-month period between Son, S. M., & Jang, S. H. (2012). Limb apraxia in a patient 293
244 thirty and thirty-one months after stroke onset. Using with cerebral infarct: Diffusion tensor tractography study. Neu- 294

245 DTT and TMS, we demonstrated that motor recov- roRehabilitation, 30, 255-259. 295
[13] Jang, S. H. (2011). Diffusion tensor imaging studies on corti- 296
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247 Because LKA can accompany motor weakness like NeuroRehabilitation, 29, 339-345. 298
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249 bilitation, including dopaminergic drugs, diagnosis of the corticospinal tract in the brainstem of the human brain. 300

250

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LKA is important in stroke rehabilitation. Therefore,
we believe that our results have important implications
for stroke rehabilitation. However, because it is a case
[15]
or
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