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Article history: Studies about recovery from cerebellar stroke are rare. The present study assessed motor decits in the
Received 15 April 2013 acute phase after isolated cerebellar stroke focusing on postural impairment and gait ataxia and outlines
Received in revised form 12 August 2013 the role of lesion site on motor outcome, the course of recovery and the effect of treadmill training. 23
Accepted 13 September 2013
patients with acute and isolated cerebellar infarction participated. Decits were quantied by ataxia
scores and dynamic posturography in the acute phase and in a follow up after 2 weeks and 3 months. MRI
Keywords: data were obtained to correlate lesion site with motor performance. Half of the patients that gave
Cerebellar infarction
informed consent and walked independently underwent a 2-week treadmill training with increasing
Ataxia
Brain imaging
velocity. In the acute phase patients showed a mild to severe ataxia with a worse performance in patients
Treadmill training with infarction of the superior in comparison to the posterior inferior cerebellar artery. However, after 3
Voxel based lesion symptom mapping months differences between vascular territories were no longer signicant. MRI data showed that
patients with larger infarct volumes had a signicantly more severe ataxia. In patients with ataxia of
stance, gait and lower limbs lesions were more common in cerebellar lobules IV to VI. After 3 months a
mild ataxia in lower limbs and gait, especially in gait speed persisted. Because postural impairment had
fully recovered, remaining gait ataxia was likely related to incoordination of lower limbs. Treadmill
training did not show signicant effects. Future studies are needed to investigate whether intensive
coordinative training is of benet in patients with cerebellar stroke.
2013 Published by Elsevier B.V.
F indicates female; M, male; PICA, posterior inferior cerebellar artery; SCA, superior
A total of 23 patients with acute, isolated cerebellar stroke (6
cerebellar artery.
females and 17 males, mean age 58.6 13.5 yrs) and 13 healthy
age-matched controls (4 females and 9 males, mean age
59.3 10.5 yrs) were enrolled in this study. In detail, ten patients 2.2. International Cooperative Ataxia Rating Scale (ICARS)
presented with a stroke in the territory of the superior cerebellar
artery (SCA) and 13 patients had a stroke of the posterior inferior Cerebellar symptoms were quantied using the International
cerebellar artery (PICA). On initial presentation, eleven of 23 patients Cooperative Ataxia Rating Scale (ICARS) of the World Federation of
showed cerebellar lesions that included the cerebellar nuclei. Only Neurology [18]. ICARS ranges from 0 (no ataxia) to 100 (strongest
patients with an isolated cerebellar stroke were included in the study, ataxia) and comprises four main clinical core symptoms: posture
veried by an initial MRI scan. Mean duration from diagnosis of stroke and gait disturbances, kinetic functions, speech disorders and
until enrolment in the study was 12.4 11.7 (range 141) days. Most oculomotor disorders. As it has been reported previously the
of the patients and control subjects of the present study have already scores were subdivided into gait (max. score 12), posture (max.
been examined in a recent study of recovery of upper limb ataxia [10]. score 18) and lower limb (max. score 16) to describe more in
In a multicentre-study patients were recruited from the university detail the relevant ataxia for the applied methods [9]. Additionally,
hospital in Essen and ve other neurological hospitals in the the gait score was subdivided into the parameters walking
surroundings. Fig. 1 gives a detailed explanation of the relationship capacities and gait speed.
of patients of the acute stage, of the follow-up investigation and
treadmill training. A detailed description of the patients character- 2.3. Dynamic posturography
istics is given in Table 1. All subjects gave their written informed
consent prior to their inclusion in the study. The study was approved Postural stability was examined by dynamic posturography
by the local ethics committee and has therefore been performed in using the Sensory Organization Test (SOT) of the EquiTest1 system
accordance with the ethical standards laid down in the 1964 (NeuroCom Inc., Portland, OR) and might be regarded as an
Declaration of Helsinki and its later amendments. advanced version of the Romberg Test. The application of SOT for
Fig. 1. Flow chart with an explanation of the relationship of patients of the acute stage, of the follow-up investigations and treadmill training and reasons for the loss of
patients.
U. Bultmann et al. / Gait & Posture 39 (2014) 563569 565
the assessment of postural stability in cerebellar diseases has been were randomized and half of the patients underwent treadmill
described in detail previously [9,19]. The SOT measures the body training during the rst 2 weeks after enrollment in the study.
sway and comprises six different conditions with three repetitions Patients that were not able to walk alone were excluded from
for each condition. For analysis, the total sway area of the centre of treadmill training to prevent falls. This training took place
gravity was calculated based on changes in ground reaction force, additionally to a classical physiotherapy after stroke according
using custom-made algorithms. to the Bobath concept. The treadmill training was carried out by an
experienced therapist (N.F.) and lasted 30 min per day. Velocity
2.4. MR imaging during the training was varied and progressively increased
according to the patients ability.
All patients received a cranial MRI using a Siemens Sonata 1.5 T
to assess the location and size of the stroke and to exclude 2.6. Statistical analysis
extracerebellar lesions. Methods of acquisition and processing of
MRI have been described in detail previously [10]. Statistical analysis of the data was performed using SPSS 20.0.0
Additionally, voxel-based lesion symptom mapping (VLSM) (SPSS Inc., Chicago, IL, USA). Univariate ANOVA were calculated to
of the cerebellum was performed [20]. This analysis calculates assess differences between patients and controls and in post hoc
for each voxel the statistical probability that a lesion in this comparisons between the different patients groups (SCA vs. PICA
voxel is accompanied by an abnormal performance using the infarction, affected vs. unaffected cerebellar nuclei, left vs. right
permutated BrunnerMunzel rank order statistic. The statistical side) at the acute stage. Additional repeated-measures ANOVA
maps were superimposed on MRI images of a healthy brain were calculated over three points of time, i.e. the acute stage, after
(Fig. 2). 2 weeks and 3 months, to assess differences of recovery between
groups (block by group interaction effect). Because only 16 of
2.5. Rehabilitation treatment initially 23 patients were available for follow-up, a univariate
ANOVA for this group of patients was repeated for the acute stage
In order to test the usefulness and efciency of a rehabilitation and calculated for the last examination after 3 months. Level of
treatment during the acute phase after cerebellar stroke, patients signicance was set to P < 0.05.
Fig. 2. Superimposed acute lesions (a) of all 23 patients with cerebellar infarctions. Patients lesions are superimposed on a MRI of a healthy control subject and right-sided
lesions were ipped to the left. The number of overlapping lesions is indicated by the colour scale. There are two centres of lesion overlap, in the upper cerebellum,
representing the SCA territory, and in the lower cerebellum according to PICA territory. Voxel-based lesion-symptom mapping (b and c) of all 23 patients. Z-values are
indicated by the colour scale. Z-values between 2.5 and 3.2 (corresponding to P-values between 0.05 and 0.01) are shown. Analysis revealed that an area spanning vermal
lobules IV to the hemispheric lobule VI including the dentate nuclei was signicantly associated with a higher total ICARS score (b). For the ICARS subscores gait (c),
posture and lower limb, analysis showed the highest t-values in the same area. (For interpretation of the references to colour in this gure legend, the reader is referred to
the web version of the article.)
566 U. Bultmann et al. / Gait & Posture 39 (2014) 563569
Fig. 3. Comparison of the total ICARS score and its subscores for gait, posture and lower limb between patients and controls, as also between patient subgroups
regarding the stroke territory (SCA, PICA), side of infarction and involvement of cerebellar nuclei. Mean score in percent with standard error of the mean is shown. ICARS total
score and all subscores were higher in patients with SCA than with PICA infarction.
U. Bultmann et al. / Gait & Posture 39 (2014) 563569 567
ICARS score, ICARS gait and ICARS lower limb (P = 0.04, >0.99). After 3 months, no signicant difference was detected
P = 0.02, P = 0.04, respectively), but there was no difference for between patients who received treadmill training and those
ICARS posture (P = 0.12). Depending on the vascular territory, the without treadmill training for total ICARS score (P = 0.59) and for
side of infarction or involvement of cerebellar nuclei there was no the ICARS subscores (P-values >0.35).
signicant difference after 3 months (P-values >0.08).
4. Discussion
3.1.4. ICARS gait analysis
We performed an additional statistical analysis between In the acute phase after an isolated cerebellar stroke patients
patients and controls comparing walking capacities and gait speed had a mild to severe postural impairment and ataxia of gait and
as part of the gait score of ICARS. In a univariate ANOVA at the lower limbs, which was shown in the ataxia scores and in the
acute stage the group of 23 patients showed worse walking dynamic posturography. Patients with an infarction of the SCA
capacities than the group of control subjects (group effect, were more impaired than patients with an infarction of the PICA. A
P = 0.006). Comparison of the follow-up group of 16 patients with comparison of ataxia in patients with right- and left-sided
controls showed a signicant group effect at the acute stage, too infarctions and with and without an involvement of the cerebellar
(P = 0.01). After 3 months differences were no longer signicant nuclei did not show signicant differences. Secondly, the recovery
(P = 0.2). In an ANOVA with repeated measures group effect was of these motor decits within the rst 3 months after stroke was
P = 0.02, block effect P = 0.007 and block by group interaction effect high. No balance decits could be detected after 3 months, while
(P = 0.007). Analysis of gait speed at the acute stage showed a mild decits in lower limbs and gait, especially in gait speed
signicant group effect for all 23 patients (P < 0.001) and for the 16 persisted. Thirdly, by using voxel based lesion symptom mapping a
patients of the follow-up group (P = 0.01) compared to controls. correlation between the ataxia scores and a lesion in lobules IV to
After 3 months the difference between patients and controls was VI in the upper cerebellum was shown. Furthermore, patients with
still signicant (P = 0.002). An ANOVA with repeated measures larger infarct volumes had a signicantly higher total ICARS score,
over the 3 months showed a signicant group effect (P = 0.001), i.e. a more severe ataxia. Finally, additional treadmill training did
block effect (P = 0.02) and block by group effect (P = 0.02). not lead to a further improvement of the motor decits.
Because of the missing decit in the ICARS subscore posture
3.2. Dynamic posturography and in posturography in the present study after 3 months, and
persistent decits in the ICARS subscores gait and lower limb,
The ten patients that took part in the rehabilitation training and we suppose a relationship between the ataxia of lower limb and
twelve controls were included in the analysis of dynamic gait disturbances. These results are in line with previous ndings
posturography (Fig. 4). In the repeated-measures ANOVA across that disordered intra limb coordination with increased timing
the three points in time, there was a signicant greater sway area variability seemed to contribute to walking decits in patients
for patients than for controls for all six conditions together with isolated cerebellar stroke [21]. Of note, this does not exclude
(P = 0.04). There was a signicant block-effect with a general the contribution of balance decits [22,23]. Comparing patients
decrease of the sway area during the 3 months (P < 0.001). The with an infarction of the SCA or the PICA in the initial phase after
decrease in sway area was greater for patients than for controls stroke, patients with infarction of the SCA performed worse in the
over the 3 months (P = 0.04, block by group-effect). A post hoc total ICARS score as well as in all subscores. However, in the course
analysis revealed a signicant difference between patients and of the study, no differences were detected anymore. Accordingly,
controls for condition 6 (P = 0.04), where the subjects performance within the 3 months, patients with an infarction of the SCA
depends on the vestibular system. A repeated-measures ANOVA improved signicantly better than patients with an infarction of
for all six conditions as also for each condition separately did not the PICA. Most relevant structures for limb movements and gait are
show signicant differences between patients with SCA infarction located in the superior part of the cerebellum which is supplied by
compared to patients with PICA infarction, between patients with the SCA [8]. Therefore, patients with SCA infarction show more
left- and right-sided infarctions or between patients with and motor impairment than patients with PICA infarction at the acute
without involvement of cerebellar nuclei (P-values >0.07). stage. The main reason for the lack of a difference between vascular
territories after 3 months may be an adjustment of both groups by
3.3. MR imaging the good spontaneous recovery of patients with cerebellar stroke
in general. As a reason for this good recovery an activation of
The mean infarction volume on the MRI for all 23 patients was contralateral cerebellar and neocortical areas is discussed [7].
7.01 7.0 cm3 (range 0.333.7 cm3). Further analysis revealed two In the present study, no signicant difference in the functional
centres of lesion overlap: In the upper cerebellum, representing the outcome between patients with affection and without an affection
SCA territory, and in the lower cerebellum according to PICA territory of the cerebellar nuclei was shown in contrast to previous studies
(Fig. 2). The lesion in the upper cerebellar part was assigned to lobules [8,9,19]. One reason for the missing expected association may be
IV/Crus I, whereas the lower cerebellar lesion site was identied as the small sample size. Furthermore, oedema in the acute phase
lobules VII and VIII. Voxel-based lesion-symptom mapping revealed after the stroke has to be differentiated from permanent lesions
that an area spanning vermal lobules IV to the hemispheric lobule VI and oedema may have pretended an involvement of cerebellar
including the dentate nuclei was signicantly associated with a nuclei in some patients.
higher total ICARS score and subscores. In hemiparetic patients, treadmill training was performed with
increasing speed during training adapting to the personal
3.4. Rehabilitation training capability of the patients as a kind of forced induced strategy
[12]. In the present study, treadmill velocity was increased during
When comparing the two groups regarding the total ICARS training, too. The nding of a persistent reduced gait speed in
score and its subscores (treadmill-trained group N = 5 vs. no patients after cerebellar stroke justies the attempt of a training
treadmill training N = 5), there were no signicant differences (P- with increasing speed. However, no effect of treadmill training
values >0.85) on the initial exam. Over the 3 months, there was a could be shown in the present study. A possible reason for the lack
signicant block-effect (P < 0.03), but no block by group interac- of benets from the treadmill training could be, that decreased
tion effect for the total ICARS scores and its subscores (P-values velocity is not a cerebellar induced abnormality but a safety or
568 U. Bultmann et al. / Gait & Posture 39 (2014) 563569
Fig. 4. Comparison of mean sway area in cm2 between patients and controls for the six conditions of the Sensory Organization Test (SOT). In condition 1 balance function is
measured under normal sensory conditions and in condition 2 with eyes closed. During the other conditions the sensory information is varied by rotating the visual surround
(condition 3) and/or the platform on which the subject is standing (condition 4) in a sway-referenced matter. Sway-referenced corresponds to anteriorposterior motion of
the visual surround or the platform that is coupled to the subjects own sway. In condition 5 the subjects eyes are closed and the platform is sway-referenced whereas in
condition 6 both parameters are sway-referenced. Mean score of three repetitions in percent with standard error of the mean and the absolute number of falls is shown for the
acute phase (1), after 2 weeks (2) and 3 months (3). The decrease in sway area was greater for patients than for controls over the 3 months.
compensation strategy ot the patients. Another reason may be, that possibly, by increasing the declination of the treadmill or by
the spontaneous recovery after acute cerebellar stroke was high. As introducing obstacles. In the future, different therapies need to be
a further explanation, the treadmill training of the present study compared in randomized controlled trials.
might have been not challenging enough for patients with only
mild ataxia. Because of the persisting limb ataxia in the chronic Conicts of Interest
state the improvement of the intra limb coordination seems to be
important. Thereby, the efciency of a treadmill training may be The authors declare that they have no conict of interest in this
enhanced by increasing the degree of difculty of the training, study.
U. Bultmann et al. / Gait & Posture 39 (2014) 563569 569