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Fujino 2019
Fujino 2019
Fujino 2019
DOI:10.3233/NRE-192911
IOS Press
1 Electromyography-guided electrical
2 stimulation therapy for patients with
pusher behavior: A case series
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3
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4 Yuji Fujinoa,∗ , Hidetoshi Takahashib , Kazuhiro Fukatab , Masahide Inoueb , Kohei Shidab ,
5 Tadamitsu Matsudaa , Shigeru Makitab and Kazu Amimotoc
a Department
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6 of Rehabilitation, Juntendo University, Hongo, Bunkyo-ku, Tokyo, Japan
7
b Department of Rehabilitation, Saitama Medical University International Medical Center,
8 Yamane, Hidaka, Saitama, Japan
9
c Department of Physical Therapy, Tokyo Metropolitan University, Higashi-Ogu, Arakawa-ku,
10 Tokyo, Japan
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11 Abstract.
12 BACKGROUND: Pusher behavior (PB) is a posture disorder due to a subjective bias in verticality perception. However,
13 muscle activity characteristics in this disorder and the effective treatments are not known.
14 OBJECTIVE: To investigate electromyographic (EMG) activity and the effect of electrical stimulation (ES) in PB.
15 METHODS: Two PB patients were enrolled. The EMG activity was measured over the upper and lower limb muscles on
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16 the non-paretic side, and over the trunk muscles on both sides during sitting. We used a modified ABA single-case design
17 consisting of consecutive baseline, intervention, and follow-up, each phase lasting 2 d. During the intervention, together
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18 with conventional treatment, the patient received ES for 5 min/d on the muscle antagonist to the muscle where excessive
19 activity was observed. PB was assessed before and after each phase using the scale for contraversive pushing and the Burke
20 lateropulsion scale. Truncal balance was evaluated using the trunk control test.
21 RESULTS: In both patients, electromyography of the non-paretic triceps brachii muscle revealed excessive activity. To
22 inhibit the excessive activity, ES was applied to the non-paretic biceps muscle. All scores improved after the intervention and
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23 follow-up phases.
24 CONCLUSIONS: ES based on EMG activity is therapeutic for PB.
27 Some stroke patients exhibit a symptom called With respect to the processing mechanism of PB, 32
28 pusher behavior (PB). This behavior is a unique sign Karnath, Ferber & Dichgans (2000) have reported the 33
29 in which the patient collapses toward the weak side verticality perception disorder involving some direc- 34
∗ Address
body from true vertical as well as uncertainty (and 36
for correspondence: Yuji Fujino, Department of
Rehabilitation, Juntendo University, 3-2-12, Hongo, Bunkyo-ku,
thus instability) in the patient’s verticality. Under the 37
Tokyo 113-0033, Japan. Tel.: +81 3 3812 1780; Fax: +81 3 3812 assumption of a verticality perception disorder, treat- 38
1781; E-mail: y.fujino.pb@juntendo.ac.jp. ment strategies for PB have focused on the visual, 39
ISSN 1053-8135/19/$35.00 © 2019 – IOS Press and the authors. All rights reserved
2 Y. Fujino et al. / Electromyography-guided ES therapy for patients with PB
43 that prone-position therapy immediately and signifi- nosed with cardiogenic cerebral embolism in the right 61
44 cantly improves acute-phase and subacute-phase PB middle cerebral artery area (Fig. 1). Both patients also 62
45 (Fujino et al., 2016). While the mechanism of prone- suffered from motor paralysis, sensory loss, and uni- 63
46 position therapy is unknown, the fact that this therapy lateral spatial neglect (Table 1). Both patients showed 64
47 improves PB suggests that PB is not only a disorder of severe PB as shown in Table 2. The patients received 65
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48 perception of verticality, but also partly a pathology an explanation about the purpose of the study and 66
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49 of motor output and adjustment. However, currently provided their consent in writing. 67
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54 fore, this study investigated muscular activity in PB 3.1. Electromyographic measurements 69
57 the observed pattern of electromyographic (EMG) biceps brachii, triceps brachii, vastus lateralis, and 71
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58 activity. biceps femoris muscles on the non-paretic side, and
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Fig. 1. The head computed tomography scans for Case 1 are presented in the upper row, and the head diffusion-weighted magnetic resonance
imaging (MRI) scans for Case 2 are presented in the lower row. A slight hemorrhagic infarction is observed in Case 1. In both cases, the
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images show right middle-cerebral artery embolism due to cardiogenic cerebral infarction (M1 occlusion).
Table 1
Patient demographic and other characteristics
Case Age Sex Time after BRS# Severity of Severity of unilateral MMSE†
no. (y) onset (d) sensory loss* spatial neglect*
1 75 M 17 II/I/II Severe Severe 17
2 69 M 14 II/I/II Severe Severe 20
Abbreviations: BRS, Brunnstrom recovery stage; MMSE, Mini mental state examination; M, male. #BRS, Upper extremity/finger/lower
extremity. *Evaluated by stroke impairment assessment set. †Score has a total 30 points (cut-off is 23 points).
Y. Fujino et al. / Electromyography-guided ES therapy for patients with PB 3
Table 2
Changes in clinical and outcome scores
Before After After After
baseline baseline intervention follow-up
Stroke impairment assessment set
Case 1 Total 27 27 28 28
Case 2 Total 26 26 28 28
Scale for contraversive pushing
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Case 1 Total 6 6 2.5 3.5
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Posture 1/1 1/1 0.25/0.75 0.75/0.75
Extension 1/1 1/1 0/0.5 0.5/0.5
Resistance 1/1 1/1 0/1 0/1
Case 2 Total 6 6 2.5 2.5
Posture 1/1 1/1 0.25/0.25 0.25/0.25
Extension 1/1 1/1 0.5/0.5 0.5/0.5
Resistance 1/1 1/1 0/1 0/1
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Burke lateropulsion scale
Case 1 Total 14 14 6 10
Supine 2 2 0 1
Sitting 2 2 0 1
Standing 4 4 2 2
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Transfers 3 3 1 3
Walking 3 3 3 3
Case 2 Total 13 13 6 7
Supine 1 1 0 0
Sitting 3 3 0 1
Standing 4 4 2 2
Transfers 2 2 1 1
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Walking 3 3 3 3
Trunk control test
Case 1 Total 0 0 12 12
Rolling to weak side 0 0 12 12
Rolling to strong side 0 0 0 0
Balance in sitting position 0 0 0 0
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72 the rectus abdominis and erector spinae muscles bilat- condition with the hand on the non-paretic side rest- 88
73 erally. A pair of disk electrodes of diameter 10 mm ing on the seat 15 cm from the outside of the thigh, 89
74 were placed on each muscle 20 mm apart for record- and a trunk-lateral bending condition in which the 90
76 placed, the skin was degreased with an alcohol swab the hand on the non-paretic side resting on the seat 92
77 and a layer of cuticle was then removed with a skin 30 cm from the outside of the thigh. Because of the 93
78 pretreatment agent to reduce the electrical resistance severity of the PB symptom, the positions of the 94
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79 of the skin. The EMG signals were recorded using measured extremities were configured by an assis- 95
80 a Neuropack MEB-4208 (Nihon Kohden, Tokyo, tant. Participants were asked to maintain their posture 96
81 Japan). The low-pass filter was set at 20 Hz, the hi- at a predefined position as well as possible while 97
82 pass filter was set at 3 kHz, and the data were sampled measurements were being made. Measurements were 98
84 Participants sat in a seat that was adjusted to a with PB resist correction of their posture, support 100
85 height at which the knee joint was flexed at 90◦ by the assistant was minimized to avoid correcting 101
86 and the soles of the feet were flat on the floor. Two the posture when measuring and recording the EMG 102
87 measurement conditions were used: a trunk-upright activity. The EMG activity was measured 17 days 103
4 Y. Fujino et al. / Electromyography-guided ES therapy for patients with PB
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speech, and unaffected-side function (see Appendix 132
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1). PB was evaluated using the Scale for contraver- 133
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SCP subscales, and PB was considered most severe 138
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trol test (TCT; Collin & Wade, 1990) was used to 142
Fig. 2. In preparation for electrical stimulation therapy, two elec- up from a lying-down position, and sitting in a bal- 146
trodes separated by 5 cm are placed over the muscle belly of the
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anced position on the edge of the bed with the feet 147
biceps brachii.
off the ground for 30 s. The scoring is as follows: 0, 148
104 after the onset of the symptom in Case 1, and 14 days manner; and 25, able to complete the movement nor- 151
after the onset of the symptom in Case 2. mally (total score range, 0 to 100). These assessments
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105 152
108 study ABA design, and trials began the day after EMG
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109 measurements were taken for both cases. A1 (base- 4.1. Characteristics of muscle activity 156
112 a conventional physical therapy for PB was admin- showed greater muscular activity in the triceps brachii 158
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113 istered (a balance exercise in a sitting position, an on the non-paretic side in both cases. In addition, 159
114 exercise in standing up with a verticality indicator, the excessive muscle activity of the triceps was 160
115 and a walking exercise using a knee-ankle-foot ortho- more significant in the trunk-lateral bending condi- 161
116 sis, among others). In phase B, an additional five-min tion (Fig. 3). 162
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121 brachii as illustrated in Fig. 2, and the stimulus inten- cle suppresses contraction of the antagonist muscle, 165
122 sity was set to a value above motor threshold (25 mA which is the triceps brachii, by a spinal reflex. 166
123 intensity, 100 Hz frequency, and 300 s pulse width). The triceps brachii muscle on the non-paretic side 167
124 ES was applied during sitting with the trunk-upright was identified in EMG measurements as a target 168
position, maintained with assistance from a therapist. for such indirect activity modification by electrical 169
Y. Fujino et al. / Electromyography-guided ES therapy for patients with PB 5
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Fig. 3. Electromyographic findings recorded with the participant sustaining a sitting position; A and B are the voltage traces for Case 1, and
C and D are the traces for Case 2. In the trunk-upright condition, significant muscular activities are observed in the triceps in both cases.
This tendency is even more significant in the trunk-lateral (sideways-leaning) condition. The scale bars shown in A apply to all four panels.
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170 stimulation. Table 2 shows the results of applying during sitting. Consequently, the present study was 188
171 ES to the biceps to suppress muscular activity in the quite interesting in that it showed an instantaneous 189
173 The SIAS score, the comprehensive evaluation for intervention completely different from previous best 191
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174 stroke, was low for both cases and no significant practice. Previous best practice focused on manip- 192
175 changes were observed after the intervention. In the ulation of the sensory modalities used to perceive 193
176 SCP, PB scored as very severe for both cases. Both verticality. 194
177 the SCP and BLS scores were reduced immediately Paci & Nannetti (2004) reported that treatment 195
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178 by ES. In both cases, the SCP and BLS scores wors- using visual or auditory feedback resulted in imme- 196
179 ened slightly during the follow-up phase, but the PB diate positive effects for a sub-acute stroke patient. 197
180 during follow-up was nonetheless milder than during Their patients underwent physiotherapy over a 3- 198
181 the baseline phase. The TCT score was poor during week period, and the SCP score improved from 4.75 199
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182 the baseline phase for both cases; however, this score points to 2.75 points. Krewer et al. (2013) com- 200
183 improved after the intervention phase, with the result pared the immediate after-effects of three different 201
184 that both participants could sit independently. interventions (20 min per session) for PB in a cross- 202
185 5. Discussion gait training than with physiotherapy involving visual 205
186 This is the first report on the characteristics of mus- noted only on the BLS, which can detect smaller 207
187 cular activity and the effect of ES in patients with PB changes than the SCP. Yang et al. (2015) tested 208
6 Y. Fujino et al. / Electromyography-guided ES therapy for patients with PB
209 the effect of a computer-generated interactive visual EMG evaluation was not performed after ES. Third, 261
210 feedback training program in a randomized, con- although we established that the EMG findings could 262
211 trolled trial, and reported that the SCP for the be different between the sitting lateral and upright 263
212 intervention group improved by 4.0 ± 1.1 points postures, the EMG status was not investigated for a 264
213 while that for the control group improved by 1.4 ± 1.0 standing posture because of the difficulty of maintain- 265
214 points after treating patients three times a week for ing our participants standing due to severe PB. Fourth, 266
215 three weeks. Although previous studies showed that the EMG findings suggested that, in the sitting posi- 267
216 these interventions had a certain level of effect, the tion, the triceps brachii muscle on the non-paretic 268
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217 time course of PB needs to be considered. Abe et side may induce PB, but the reason could not be 269
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218 al. (2012) reported on the length of recovery from shown. Many questions remain regarding the mech- 270
219 PB and showed that PB spontaneously resolves after anism, effective treatment, etc., of PB, which merit 271
220 approximately two months even for severe cases. In further research. 272
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223 which suggests that the observed recovery was due
224 to ES. Conflict of interest 273
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275
227 originating from a muscle spindle of an agonist mus-
228 cle propagates through the 1a nerve fiber, activating
229 alpha motor neurons of the same agonist muscle while
230 at the same time deactivating the motor neurons of the References 276
231 antagonist muscle via a spinal inhibitory interneuron.
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232 Deactivation by this mechanism is known as recip-
Abe, H., Kondo, T., Oouchida, Y., Suzukamo, Y., Fujiwara, S., 277
233 rocal inhibition. PB is abnormal movement in the Izumi, S. (2012). Prevalence and length of recovery of pusher 278
234 “non-paretic side” of upper and lower limbs (ipsilat- syndrome based on cerebral hemispheric lesion side in patients 279
235 eral hemisphere) and is not caused by brain damage as with acute stroke. Stroke, 43, 1654-1656. 280
236 is the case for spasticity (contralateral hemisphere). Baccini, M., Paci, M., Nannetti, L., Biricolti, C., Rinaldi, L. A. 281
237
diagnosing “pusher behavior” and construct validity. Physical 283
238 reflex pathway. Therapy, 88, 947-955. 284
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239 However, it remains unclear why changes in local Collin, C. & Wade, D. T. (1990). Assessing motor impairment after 285
240 muscle activity improved balance ability. Wolpert et stroke: A pilot reliability study. Journal of Neurological and 286
241 al. proposed a comparator model in which changes Neurosurgical Psychiatry, 53, 576-579. 287
D’Aquila, M. A., Smith, T., Organ, D., Lichtman, S., Reding, M. 288
242 in the external world that accompany an exercise
(2004). Validation of a lateropulsion scale for patients recov- 289
243 are detected by somatic and visual senses and are ering from stroke. Clinical Rehabilitation, 18, 102-109.
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290
244 then fed back to the brain where a sensory predic- Fujino, Y., Amimoto, K., Sugimoto, S., Fukata, K., Inoue, M., 291
245 tion and the actual sensation are compared (error Takahashi, H., Makita, S. (2016). Prone positioning reduces 292
246 detection) (Wolpert, Ghahramani & Jordan, 1995). severe pushing behavior: Three case studies. Journal of Phys- 293
248 correct this error (Imamizu et al., 2000). In other Pütz, B., & Kawato, M. (2000). Human cerebellar activity 296
249 words, PB is considered to stem from impairment reflecting an acquired internal model of a new tool. Nature, 297
250 of error learning that normally corrects movements 403, 192-195. 298
251 that are erroneous due to vertical misperception. The Johannsen, L., Broetz, D. & Karnath, H. O. (2006). Leg orientation 299
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255 sensory prediction and actual sensation per the com- Karnath, H. O., Johannsen, L., Broetz, D., Ferber, S, Dichgans, J. 304
256 parator model. We conclude that ES based on EMG (2002). Prognosis of contraversive pushing. Journal of Neu- 305
311 Paci, M. & Nannetti, L. (2004). Physiotherapy for pusher behavior Tsuji, T., Liu, M., Sonoda, S., Domen, K. & Chino, N. (2000). The 320
312 in a patient with post-stroke hemiplegia. Journal of Rehabili- stroke impairment assessment set: Its internal consistency and 321
313 tation Medicine, 36, 183-185. predictive validity. Archives of Physical and Medical Rehabil- 322
314 Paci, M., Nannetti, L. & Lombardi, B. (2011). Fear of falling in itation, 81, 863-868. 323
315 stroke patients with pusher behavior. Italian Journal of Phys- Wolpert, D. M., Ghahramani, Z. & Jordan, M. I. (1995). An internal 324
316 iotherapy, 1, 12-16. model for sensorimotor integration. Science, 269, 1880-1882. 325
317 Pérennou, D. A., Mazibrada, G., Clauvineau, V., Greenwood, R., Yang, Y. R., Chen, Y. H., Chang, H. C., Chan, R. C., Wei, S. 326
318 Rothwell, J., Gresty, M. A. & Bronstein, A. M. (2008). Lat- H., Wang, R.Y. (2015). Effects of interactive visual feedback 327
319 eropulsion, pushing and verticality perception in hemisphere training on post-stroke pusher syndrome: A pilot randomized 328
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stroke: A causal relationship? Brain, 131, 2401-2413. controlled study. Clinical Rehabilitation, 29, 987-993. 329
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8 Y. Fujino et al. / Electromyography-guided ES therapy for patients with PB
330 Appendices
Appendix 1
Stroke impairment assessment set
Upper extremity Lower extremity
Motor function
Proximal 0–5 (Finger function) 0–5 (Hip flexion)
0–5 (Knee extension)
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Distal 0–5 (Knee-mouth) 0–5 (Foot tap)
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Muscle tone
DTR 0–3 0–3
Tone 0–3 0–3
Sensory function
Touch 0–3 0–3
Position 0–3 0–3
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Range of motion 0–3 Shoulder abduction 0–3 Ankle dorsiflexion
Pain 0–3 Trunk
Verticality 0–3
Abdominal MMT 0–3
Higher cortical function
Visuospatial 0–3
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Speech 0–3
Function of unaffected side
Grip strength 0–3
Quadriceps MMT 0–3
Total score 76
Abbreviations: DTR, deep tendon reflex; MMT, manual muscle testing.
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Appendix 2
Scale for contraversive pushing
A Posture (symmetry of spontaneous posture) Sitting Standing
Score 1 = severe contraversive tilt with falling to the contralesional side
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maximum = 2
C Resistance (resistance to passive correction of posture to an upright position)b Sitting Standing
Score 1 = resistance is shown
Score 0 = resistance is not shown
maximum = 2
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Total (maximum = 6)
a Forsitting, ask the patient to glide the buttocks on the mattress toward the nonparetic side, to transfer from bed to wheelchair toward the
nonparetic side, or both. For standing, ask the patient to start walking. If pushing already occurs when the patient is rising from the sitting
position, section B is given the value of 1 for standing. b Touch the patient at the sternum and the back. Give the following instructions: “I
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Appendix 3
Burke lateropulsion scale
Spine
Use the ‘log roll’ technique to test patient’s response. Roll first towards the affected side, then towards the unaffected side. Circle the
side to which the resistance is most prominent. Score below the maximum resistance felt and add one point if resistance is noted in
both directions. (Patients with marked lateropulsion may resist rolling to either side, hence an extra point is added if resistance is
noted with rolling both towards and away from the affected side).
0 = No resistance to passive rolling.
1 = Mild resistance.
2 = Moderate resistance.
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3 = Strong resistance.
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4 = One point added because resistance was noted in both directions.
Sitting
Score with the patient seated, feet off floor, with both hands in lap. The expected hemiplegic response is for patient to carry his weight
towards the unaffected side. Some patients will passively fall towards their paretic side when placed in true vertical position by the
examiner. This will not be scored as ‘lateropulsion.’ Position the patient with their trunk 30 degrees off true vertical towards their
affected side, then score the patient’s response to your attempts to bring them back to vertical. The ‘lateropulsion’ phenomenon is
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an active attempt by the patient to keep their center of gravity towards their impaired side as they are brought to true vertical.
0 = No resistance to passive return to true vertical sitting position.
1 = Voluntary or reflex resistive movements in trunk, arms or legs noted only in the last five degrees approaching vertical.
2 = Resistive movements noted but beginning within 5 to 10 degrees of vertical.
3 = Resistive movements noted more than 10 degrees off vertical.
Standing
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Score with the patient standing with whatever support is needed. The expected hemiplegic response is for the patient to carry their
weight toward the unaffected side or to passively fall towards their paretic side when placed in true vertical position by the
examiner. This will not be scored as ‘lateropulsion.’ Position the patient with their trunk 15 to 20 degrees off true vertical towards
their affected side then score the patient’s response to your attempts to bring them back to vertical, then 5 to 10 degrees past
vertical toward the intact side. The ‘lateropulsion’ phenomenon is a voluntary or reflexive response in the trunk or limbs to keep the
center of gravity towards the impaired side, e.g., forced trunk curvature towards the paretic side, flexion of the affected hip or knee,
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or shifting weight to the lateral aspect of the unaffected foot.
0 = Patient prefers to place his center of gravity over the unaffected leg.
1 = Resistance is noted when attempting to bring the patient 5 to 10 degrees past midline.
2 = Resistive voluntary or reflex equilibrium responses noted, but only within 5 degrees of approaching vertical.
3 = Resistive reflex equilibrium responses noted, beginning 5 to 10 degrees off vertical.
4 = Add one point if resistance noted in both directions.
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Transfers
Score this function by transferring the patient from the seated position first to the unaffected side, then if possible, to the affected
side. The expected hemiplegic response would be for the patient to require more assistance to transfer towards the affected side
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(use a sit pivot, modified stand pivot, or stand pivot transfer, depending on the patient’s functional level).
0 = No resistance to transferring to the unaffected side is noted.
1 = Mild resistance to transferring to the unaffected side.
2 = Moderate resistance to transferring is noted. Only one person is required to perform the transfer.
3 = Significant resistance is noted with transferring to the unaffected side and two or more people are required to transfer the patient
due to the severity of lateropulsion.
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Walking
Score lateropulsion by noting active resistance by the patient to efforts by the therapist to support the patient in true vertical position.
Do not score passive falling or leaning to the paretic side. Score lateropulsion as follows:
0 = No lateropulsion noted.
1 = Mild lateropulsion noted.
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