Acta Neuro Scandinavica - 2010 - Johansson - Current Trends in Stroke Rehabilitation A Review With Focus On Brain
Acta Neuro Scandinavica - 2010 - Johansson - Current Trends in Stroke Rehabilitation A Review With Focus On Brain
Review Article
Current trends in stroke rehabilitation.
A review with focus on brain plasticity
Johansson BB. Current trends in stroke rehabilitation. A review with B. B. Johansson
focus on brain plasticity. Department of Clinical Neuroscience, Wallenberg
Acta Neurol Scand: 2011: 123: 147–159. Neuroscience Center, Lund University, Lund, Sweden
2010 John Wiley & Sons A ⁄ S.
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compared with general medical ward care (20–22). has attained much media interest after a significant
Also cognitively impaired stroke patients do ben- effect was obtained in a randomized study with a
efit from admission to an acute stroke unit (23). 2-week program of CIMT applied to 222 stroke
These data have been supported by a large study patients mostly with mild to moderate impairment
including 105,043 patients with acute stroke 3–9 months after stroke (33). A follow-up
reported to the Swedish Stroke Register during 24 months after the ischemic event showed a
the years 2001 through 2005 that were followed persistent benefit (34). Some limitations with the
until January 2007 (24). Stroke unit care was study include that the controls received ‘‘usual and
associated with reduced risk for death and institu- customary care’’ that involved less motor training
tional living at 3 months after stroke onset, and than that delivered to the CIMT group. Further-
with better long-term survival in all subgroups more, the separate effects of higher dose of motor
(age, sex, stroke subtypes, and level of conscious- training and immobilization cannot be evaluated.
ness). The benefit of stroke units compared to The study included rather few patients with severe
general wards is most likely a combination of impairments, and the participating patients may
optimal medical and nursing care, task oriented, have represented a minority of patients with
and for the individual meaningful training in an chronic stroke (35). A remaining question is
environment that gives them confidence, stimula- whether it is superior to other treatment of
tion, and motivation (25). Mere admittance to a comparable intensity.
stroke unit with specially trained staff encouraging There is no evidence that CIMT is of benefit in
active participation in the rehabilitation process early stroke rehabilitation. No significant differ-
and more information to patients and relatives ences were noted in patients randomized within
may increase the motivation and expectation of the 2 weeks after stroke either to 2 weeks of CIMT or
patients. Animal studies have demonstrated that to traditional therapy at an equal frequency of up
environmental enrichment has many functional to 3 h ⁄ day. The groups were well balanced for
and biological effects and significantly enhance the frequency, duration, and intensity of the treatment,
effect of other interventions (2, 5, 26, 27). and the results did not show any significant
differences between the groups (36). In another
study, patients were randomized within 28 days of
Motor rehabilitation
admission into three groups. Control treatment
Tactile sensibility of the hand is essential for consisted of 1 h of activity of daily living retraining
identifying objects and for motor performance. and 1 h of bilateral training 5 days a week during
When sensory perception is affected in stroke, 2 weeks, The standard CIMT group received 2 h of
rehabilitation of motor skills is more difficult to shaping therapy and wore a mitten 6 h a day; and
achieve (28). Aging is associated with reduced high intensity CIMT underwent 3 h of shaping
tactile discrimination and deterioration of fine therapy and mitten 90% of waking hours. Stan-
manipulative movements and handling of tools. dard CIMT was equally effective but not superior
Sensory stimulation by means of tactile co- to an equal dose of traditional therapy (37), and
activation of fingertips successfully improves tactile the higher intensity CIMT resulted in less improve-
acuity in elderly individuals and, in contrast to ment at 90 days. These two studies on early CIMT
motor training, it does not require active partic- emphasize the need for control groups that match
ipation or attention of the subjects. This lead to therapy intensity and dose in clinical trials.
the suggesting that it might be a useful therapeu- A meta-analysis based on 10 studies of robot-
tic intervention to improve the activity of daily assisted therapy on motor and functional recovery
living in stroke patients with impaired sensory in patients with stroke involving 218 patients
motor abilities (29, 30). A preliminary study on showed a significant effect on motor recovery of
four individual post-stroke showed that all the upper paretic limb but no significant effect on
improved in sensory tasks and motor perfor- functional ability. The recommendation was that
mance, effects that remained 4 weeks post treat- future research on the effect should distinguish
ment (31). If those data can be confirmed in between upper and lower robotics arm training and
larger studies, it may have a considerable impact concentrate on kinematic analysis to differentiate
in stroke rehabilitation. between genuine upper limb motor recovery and
Constraint-induced movement therapy (CIMT) functional recovery owing to compensation strat-
is a method in which a splint is applied to the intact egies by proximal control of the trunk and upper
hand 90% of the day to force the use of the paretic limb (38). Similarly, a Cochrane report based on 11
hand, and combined with ‘‘shaping’’ by which the trials with 328 participants found no significant
tasks are made progressively more difficult (32). It improvement in activities of daily although arm
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Stroke rehabilitation
motor function and arm motor strength improved However, the anesthetic procedure is not easy,
(39). Rehabilitation program may require different which explains why this intervention has not been
therapy protocols and equipment in acute and much used.
chronic stages of recovery (40, 41). Adding virtual Another approach is based on the concept of
reality to robot-based gate training (42) and arm interhemispheric inhibition. The cortical sensory
(43) training may have beneficial effects as will be and motor representation of the hand exerts
discussed later. inhibitory influences on the homonymous repre-
Bilateral coordination is important in daily life. sentation in the opposite hemisphere (50), an
Bilateral arm training (BAT) may be of value interhemispheric inhibition that is thought to
particular for stroke patients with severe func- contribute to skilled motor performance. Short-
tional deficits (44). In a randomized controlled term ischemic nerve block to the hand leads to
trial 6–67 months after stroke onset, BAT functional reorganization in the de-afferented
improved the spatiotemporal control of the motor cortex, and also to functional changes in
affected arm in both bilateral and unilateral homotopic motor regions in the contra-lateral
tasks and reduced motor impairment (45). Com- cortex (51, 52). Based on the observation of an
paring CIMT, BAT, and a control intervention of abnormally high interhemispheric inhibitory drive
equally intense but less specific therapy for from the motor cortex of the intact hemisphere to
2 hours a day 5 days a week for 3 weeks, both the injured hemisphere during a voluntary move-
CIMT and bilateral arm training resulted in better ment of the paretic hand in patients with sub-
performance than the control intervention. BAT cortical infarcts, it was hypothesized that this
exhibited greater gains in the proximal upper limb abnormality might adversely influence motor
than the other two groups on motor performance, recovery (53). Different neurophysiologic strate-
and CIMT produced greater functional gains in gies to increase the activity of the injured area
hand functions in patients with mild to moderate have been proposed mainly using transcranial
chronic hemiparesis (46). It has been proposed magnetic stimulation, TMS (54, 55), and trans-
that bilateral training is a necessary adjunct to cranial direct current stimulation, tDCS (56).
unilateral training and that individuals at all level Lower frequencies of repetitive TMS (rTMS = a
of severity can benefit from bilateral training train of TMS pulses of the same intensity) in the
although not all approaches are effective at all range 1 Hz range suppress excitability of the
severity levels (47). Specific training approaches motor cortex, while 20 Hz lead to a temporary
need to be matched to the individual case increase in cortical excitability (57). With tDCS, a
characteristics. To achieve bilateral skills impor- weak polarizing electrical current is delivered to
tant in daily life training should not be either the cortex, and the effect depends on the polarity
unilateral or bilateral but both. In a systematic (56). An excitatory effect is obtained with the
review based on 56 studies 1979–2008, the authors anode placed over the motor cortex, and inhibi-
concluded that the current evaluation scales are tion is induced with the cathode over motor
not optimal for exploring changes in real life of cortex. tDCS is easier to apply and less expensive
the patients and that there is a need for the than TMS, and a feasibility study demonstrated
development of direct measures of arm use in that the participants could not distinguish tDCS
real-life environments (48). from sham stimulation, making it suitable for
larger double-blinded, sham-controlled random-
ized trials (58).
Electrical brain stimulation
Two main approaches to alter the hemispheric
After a cortical lesion, the surrounding intact tissue dominance have been used in clinical studies. 1)
has an inhibitory action on the damaged area, an Reducing the cortical activity on the intact side by
intra-hemispheric inhibition. Most patients with low frequency rTMS (59–61) or by reducing the
stroke have better function in the upper arm than somatosensory input to the intact hemisphere (62,
in the hand, and it was postulated that intracortical 63); 2) Enhancing the activity in the damaged
competition from surrounding areas had an inhib- hemisphere by high-frequency rTMS (64), anodal
itory effect on the hand muscles. When the upper tDCS (58, 65), or increasing the sensory input by
part of the brachial plexus was anaesthetized, electrical stimulation of the peripheral nerves in the
intense training of the paretic hand significantly paretic hand (66–68). These manipulations have
enhanced motor function, and the improvement shown 10–30% significant effects in behavioral test
was associated with an increase in TMS-evoked in these pilot studies. Combining peripheral nerve
motor output to the practiced hand muscles. The stimulation with tDCS can facilitate the beneficial
effect remained at follow-up 2 weeks later (49). effects motor performance beyond levels reached
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Stroke rehabilitation
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virtual reality setting are promising. The patients able to sing the text of a song while they are unable to
have to be positive to VR training, continued speak the same text. When allowed to sing and speak
contact with a therapist is essential, and it needs to along with an auditory model, aphasics repeat and
be further evaluated for long-term gains. A low recall more words when singing than when speaking
cost multiple users VR environment system has (131). The intelligibility and naturalness of the
been developed for rehabilitation of patients with speech improved after vocal exercises and singing
stroke (112). training in patients with non-fluent aphasia after
stroke or trauma (132).
Intensive melodic intonation therapy for aphasia
Speech and language rehabilitation
is an old method that has been systematically
The brain organization for language involves a applied and evaluated in recent years (133, 134).
combination of cortical structures and white The method includes three important components:
matter tracts, some of which are unilateral and melodic intonation, intense training 1.5 h ⁄ d 5 days
other bilateral. A dorsal stream, ‘‘sound to action’’ a week, and simultaneous tapping with the left
(non-fluent or Broca¢s aphasia), is essentially left hand to prime the sensorimotor and premotor
oriented in most persons, and a ventral stream, cortices on the right side for articulation. Melodic
from ‘‘sound to meaning’’ (semantic aphasia), is to intonation therapy delivered at high intensity to
a considerable extent bilateral (113, 114). The patients with chronic severe Broca¢s aphasia leads
degree of language lateralization determines sus- to remodeling of the right arcuate fasciculus, a
ceptibility to unilateral brain lesions (115). fiber bundle that combines the anterior and pos-
Aphasia or dysphasia can be caused by cortical terior language area in the left hemisphere demon-
lesions and ⁄ or to damage to white matter tracts strating that plasticity can be induced in the
connecting different language areas. Decreased contra-lateral homolog tract (135).
fMRI activation was observed in the remaining Constraint-induced aphasia therapy (CIAT) is a
language area during the first days after stroke different approach. Based on the concept of
(acute phase followed 10 days later by an activa- constraint-induced therapy for motor therapy, it
tion of homolog regions in the right hemisphere. In was hypothesized that gestures and other types of
the chronic phase (about a year later), the activity non-speech communication should be prevented,
had reappeared in the remaining left language and patients forced to use speech while a therapist
areas in patients with good recovery (116). How- is playing language games with two or three
ever, there is a large variability of language aphasic patients. The picture cards and the hands
recovery after first-ever stroke, and a follow-up are hidden for other players to prevent visual
study 90 days after stroke onset failed to identify input, and all communication, mainly questions
any prognostic factors (117). Several studies indi- and answers, have to be performed by spoken
cate that both hemispheres can be involved in the words and sentences. The game is getting more
recovery process. difficult in small steps and reinforcement is pro-
Language and actions are closely linked in the vided. Extensive training 3 h a day resulted in
brain (118–120), and Broca¢s area, traditionally significant effect compared to standard training
looked upon an exclusive language area, is now one hour a day during an extended period adding
thought to detect and represent complex hierar- up to the same total amount of training, thus the
chical dependencies regardless of modalities and same training time spread over a longer time (136).
use including gesture, action and music (121–124). In a study when all aphasia patients were trained
Listening to speech specifically modulates the with CIAT over a 2-week period 1–9 years after
tongue muscles (125) and language perception stroke, half of the patients received additional
activates the hand motor cortex (126). Integrating training in everyday communication with the
observed facial movements into the speech percep- assistance of family members. Language tests
tion process involves a network of multimodal improved after training in both CIAT groups. No
brain regions associated with speech production alterative treatment group was included. However,
that contribute less to speech perception when only only the patients who were encouraged by their
auditory signals are present (127). Gestures may relatives to be more active verbally during the
facilitate word retrieval in aphasia (128). 2- week training period exhibited more communi-
There is a bihemispheric network for vocal cative activity than before treatment when
production regardless of whether the words ⁄ re-examined after 6 months (137), demonstrating
phrases are intoned or spoken (129), and words that environmental encouragement is essential
and melody are intertwined in singing (130), which for transforming the effects observed in language
may explain why some patients with aphasia are tests into useful verbal communication. For en
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Stroke rehabilitation
extensive review on the theory and practice of composite score based on four subtests of
CIAT, see review by Pulvermuller and Berthier NIHSS was almost as good as the MMSE in
(138). detecting severe cognitive impairment (147).
Using MEG (magneto-encephalography) before, Neglect is an important prognostic factor.
direct after and 3 months after the training, three Among 138 patients with stroke aged 70–91 ,
patterns of behavioral and neurophysiologic visual neglect was present in 15% 20 months after
response to constraint-induced language therapy, stroke (141). Cognitive impairment was twice as
not described in detail, were observed (139). common in patients with neglect and three times
Patients with initial response who maintained the as common in those with severe neglect, indicating
gains at 3 months exhibited an increase in left that early rehabilitation of neglect might have
temporal activation (responders, n = 8). Patients important long-term effects.
with initial significant response to the therapy but In a review based on 78 published quantitative
no effect at 3- month follow-up had greater right- and qualitative studies reporting social conse-
hemisphere activation than other patients at all quences after stroke in patients <65 years of age,
MEG sessions (lost-response, n = 4). Those who the proportions for return to work ranged from
did not improve at any time had increased acti- 0% to 100%. A negative impact on family
vation in left parietal areas (non-responders, relationships ranged from 5% to 79% and for
n = 11). deterioration in leisure activities from 15% to
Deficits in auditory single word and sentence 79%. The review highlights the need for robust and
comprehension correlate with the degree of dis- consistent methodologies in future studies on the
ruption of left-right anterior-lateral superior tem- prevalence of social problems and of the effect of
poral cortical connectivity and with local interventions to address them (148).
activation in the superior temporal cortex (118). Attention is closely related to cognition and is
Voxel-based lesion-symptom mapping has con- also important for motor skill training. A signif-
firmed the necessary role for the left anterior icant reduction in the attention deficit was
temporal lobe in mapping concepts to words (140). observed at 5 weeks and 6 months in a recent
Also aphasia related to frontal lesions can include randomized controlled trial with an attention-
semantic components. More studies that specify training program starting within 2 weeks after
the location and extension of the lesions and the stroke onset (149). The study included 78 patients
related language problems as to speech fluency and with stroke identified via neuropsychological
understanding in daily life situations are needed. assessment as having attention deficit. If these
results can be confirmed in further studies, they are
likely to have effects both on motor and cognitive
Rehabilitation of other cognitive deficits
rehabilitation and may improve quality of life after
Post-stroke cognitive impairment interferes with stroke.
recovery and is a major problem for social Whether rTMS and tDCS can influence cogni-
rehabilitation and post-stroke quality of life at tive deficits after stroke has so far been little
all ages (141–143). Cognitive activation is clearly explored. In healthy individuals, tDCS may
involved in several examples of multisensory improve language learning (150–152) and enhance
interactions already referred to including the planning activity (153). There is some evidence that
effect on neglect in VR training. Although early it may improve naming in aphasia (154, 155),
bedside cognitive assessment is possible in most working memory (156), and attention (157) in
cases (144), specific cognitive rehabilitation is often patients with stroke. These are all small studies
neglected in the early stage after stroke. Two week with no long-term follow-up.
after a first-ever ischemic infarct, 91.5% of 177
patients (mean age 50 16 years) failed in at least
Music therapy
one cognitive domain, predominantly in working
memory, episodic memory, and executive func- Listening to rhythm activates motor and premotor
tions, compared with education and age-matched cortices (158–160). Rhythmic auditory stimulation
control subjects (145). Cognitive dysfunction was and musical motor feedback can improve gait
associated with age, low level of education, NIHSS (161–163) and arm training after stroke (164, 165).
score at day 15, and middle cerebral artery Music-supported finger and arm training that
infarcts, suggesting that simple criteria may be a significantly improved function was accompanied
useful tool for designing clinical trials. (146). In by electrophysiological changes, indicating better
another study on 149 stroke patients 70+ were cortical connectivity and improved activation of
investigated after 18 months suggested that a the motor cortex (166).
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Johansson
Music is a multimodal stimulus with a well- for poor outcome among survivors of aneurismal
established role in cultural and social communica- subarachnoid hemorrhage (177). There are likely
tion and emotional well-being. During the last to be other genetic differences that can influence
years, a number of studies have demonstrated that outcome.
music listening activates many brain structures
related to sensory processing, attention, and
Concluding remarks
memory and can stimulate complex cognition
and multisensory integration (158, 167). To what Progress of time is an independent covariate that
extent these effects can be transferred to thera- reflects spontaneous recovery of functions that
peutic interventions in patients with stroke is occur during the first months after a stroke. To
currently investigated. Patients with neglect show avoid the confounding effect of time (178), most
enhanced visual awareness associated with studies testing new rehabilitation methods involve
increased fMRI activation of regions related to patients with chronic stroke several months after
emotion and attention while they listen to music stroke onset. Optimal benefits for the patients and
they like but not to un-preferred music or silence the society would supposedly be obtained by
(168). Music therapy improves executive function successful interventions in the subacute phase of
and emotional adjustment in traumatic brain stroke as indicated by the beneficial effect on
injury rehabilitation (169). It has been reported motor outcome in stroke units. Rehabilitation
to improve attention and verbal memory in program may require different therapy protocols
patients with stroke (170). However, the statistical in acute and chronic stages of recovery, and we
analyses of the data were not adequate, and need to know the optimal time for specific inter-
further studies are needed. Merely listening to ventions. More homogenous groups of patients
music and speech after stroke starting 1 week after need to be studied. Although it has been repeatedly
stroke onset induced long-term plastic changes in shown that the integrity of the corticospinal tracts
early sensory processing that correlated with the is of main importance for a favorable outcome
improvement in verbal memory and focused after stroke (7–11), the information is lacking in
attention both in music and in speech listening most studies. Cognitive rehabilitation programs
(171). A community-based intervention program starting early after stroke are essential to establish
combining rhythmic music and a specialized reha- whether attention-training, music, and other cog-
bilitation program during 8 weeks resulted in a nitive interventions can lead to better social
wider range of motion and flexibility, more adjustment and quality of life post stroke.
positive moods as well as an increased frequency
and quality of interpersonal relationships com-
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