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Restorative Neurology and Neuroscience 32 (2014) 233–245 DOI 10.3233/RNN-130315 IOS Press

Effects of balance and gait rehabilitation in cerebellar disease of vascular or degenerative origin Antonio Nardonea,b,∗ , Anna Maria Turcatoa and Marco Schieppatic,d a Posture and Movement Laboratory, Division of Physical Medicine and Rehabilitation, Scientific Institute of Veruno (NO), Fondazione Salvatore Maugeri (IRCCS), Veruno (NO), Italy b Department of Translational Medicine, University of Eastern Piedmont, Novara, Italy c Centro Studi Attivit´ a Motorie (CSAM), Fondazione Salvatore Maugeri (IRCCS), Scientific Institute of Pavia, Pavia, Italy d Department of Public Health, Experimental and Forensic Medicine, University of Pavia, Pavia, Italy

Abstract. Purpose: To investigate whether the response to rehabilitation differs between patients with abnormalities of balance and gait due to vascular or to degenerative cerebellar disease. Methods: We reviewed the outcome of 27 cerebellar patients. Fourteen patients with vascular and 13 with degenerative cerebellar disease underwent a 3-week inpatient physical therapy program for 5 days/week, 90 min/day, focused on balance and gait. Body sway area during quiet stance with eyes open and eyes closed, and gait velocity, stride length, cadence and step width were recorded. The Berg Balance Scale (BBS) and Functional Independence Measure (FIM) were administered. All tests were performed before and after treatment. Results: Before treatment, both groups showed comparable values in all sway and gait variables and in BBS. FIM score was higher in degenerative than vascular patients. After treatment, a significant reduction of body sway area was observed under both visual conditions in both groups. Gait velocity, stride length and step width improved more in the vascular than in the degenerative patient group. BBS improved in both groups. FIM improved to a larger extent in the vascular patients. Conclusion: Short-term treatment may not be sufficient to produce definite improvement in locomotion in degenerative as much as occurs in vascular patients, even if clinical and functional signs of balance improve in both groups. Keywords: Cerebellum, balance, gait, rehabilitation

1. Introduction Balance and gait control depends heavily on cerebellar function (Bastian, 2011; Manzoni, 2007). Cerebellar damage typically leads to ataxia with limb incoordination and unsteadiness of gait and balance ∗ Corresponding author: Prof. Antonio Nardone, MD, PhD, Division of Physical Medicine and Rehabilitation, Fondazione Salvatore Maugeri (IRCCS), Scientific Institute of Veruno, & Department of Translational Medicine, University of Eastern Piedmont, Novara, Italy, Via Revislate 13, 28010 Veruno (NO), Italy. Tel.: +39 0322 884930; Fax: +39 0322 884921; E-mail: [email protected].

(Morton and Bastian, 2007), increasing the risk of falls (Van de Warrenburg et al., 2005). As pharmacological treatment appears to have little effect on ataxia (Trujillo-Mart´ın et al., 2009), rehabilitation represents an alternative to help reduce motor impairment (Bultmann et al., 2013; Ilg et al., 2009, 2010; Marsden and Harris, 2011; Martin et al., 2009; Perlman, 2004; Watson, 2009). However, studies on the effects of rehabilitation in these patients are few and the results somewhat limited and controversial (Martin et al., 2009). There is non-homogeneity in cerebellar patients, as evidenced by the nature of disease

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or clinical presentation at start of treatment, or the ability to learn new motor tasks (Burgui`ere et al., 2010; G´omez-Beldarrain et al., 1998; Ioffe et al., 2006; Maschke et al., 2004; Seidler, 2010; Synofzik et al., 2008; Timmann et al., 2010), blurring the importance of the benefit gained from therapeutic exercises (Bastian, 2008; Deuschl et al., 1996). Moreover, the ability of the cerebellum to help control balance and gait and subserve motor learning may be related to the extent of spared regions (Richter et al., 2005): degenerative diseases diffusely affect cerebellar structures (Sanes et al., 1990), while vascular lesions are often circumscribed (Ioffe et al., 2006). Another confounding factor is the different natural progression of the disease between degenerative ataxias, which are steadily progressive (Klockgether et al., 1998), and disorders of vascular origin, which frequently recover well (Kelly et al., 2001). Finally, as outcome measures several studies assessed the changes in subjective indexes of balance and gait after rehabilitation with respect to baseline condition (Balliet et al., 1987; Gialanella et al., 2005; Karakaya et al., 2000), rather than using operatorindependent instrumental evaluations (Ilg et al., 2007, 2009; Morton and Bastian, 2004; Stolze et al., 2002). Here, we compared the effects of balance and gait rehabilitation on patients with degenerative vs. vascular lesions suffering from balance and gait disorders, which had been admitted in our institute in the recent past. Our aim was to assess whether, at least in the short-term, a similar intensive rehabilitative treatment of balance and gait might produce an analogous effect in patients with comparable impairment at the admission in spite of different nature of the cerebellar disorder.

had been approved by the institutional ethics committee. Inclusion criteria were a primary indication for admission to rehabilitation due to past hemorrhage or infarction, or to complex disability from degenerative disease. Altogether, the patients presented with the clinical hallmarks already described (Stolze et al., 2002), and the two groups had similar impairment of balance and gait on admission (Table 2). Exclusion criteria were: clinically-assessed peripheral sensory impairment, multiple sclerosis, tumor, hemiplegia, spasticity, absence of neuroimaging reports (Kelly et al., 2001). Sixteen patients (6 degenerative and 10 vascular) walked with an assistive device: these performed the gait evaluations prior to and after treatment with their walking aid. No patient took drugs for the treatment of ataxia or hypnotics (Allain et al., 2005) or drugs known to affect attention or sensory and motor functions (Lord et al., 1992). 2.2. Physical therapy The treatment consisted of one 90 min-session per day, 5 days a week, for 3 weeks. Since among the consequences of both vascular and degenerative disease are appearance of ataxia of balance and gait, the same usual care program was adopted for all the patients. Minor changes in the intensity and duration of distinct balance and gait exercises were tailored according to individual’s needs or capacities, and targeted according to the following exercise categories: 1) static balance, 2) dynamic control, 3) gait training, 4) flexibility and strength training. The Appendix reports details of the exercises. 2.3. Evaluation of balance and gait

2. Methods 2.1. Participants We retrospectively reviewed the outcome of 27 cerebellar patients (18 M, 9 F, mean age 59.8 yrs ± 18.1, SD) with disorders of balance and gait. Thirteen patients were affected by degenerative disease (7 M, 6 F, mean age 56.0 yrs ± 18.2) and 14 by cerebellar stroke (11 M, 3 F, mean age 63.3 yrs ± 18.0) (Table 1). Patients had been admitted to the NeuroRehabilitation Department of the Scientific Institute of Veruno. The evaluations were conducted in conformity with the Declaration of Helsinki and the procedures

All patients underwent stabilometric and baropodometric gait evaluations as well as functional evaluations. Baseline evaluations were performed on the same day, prior to treatment. The post-treatment evaluation was performed on the day following the last session. All patients completed the entire rehabilitation program. 2.3.1. Stabilometry As a measure of postural stability, body sway was recorded by means of a force platform (Win-Posture, Medicapteurs France SAS, Les Espaces de Balma, 18 avenue Charles de Gaulle, Bˆat. 33/34, 31130 Balma, France). Patients stood barefoot with eyes open (EO)

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Table 1 Clinical data of the patients Patient

Sex

Age (years)

Time since onset (months)

1 2 3 4 5 6 7 8 9 10 11 12 13 a b c d e f g i m n o p q r

F F F F M M F M F M M M M M M M M M F M M M M M F M F

63 50 81 59 68 60 77 16 57 38 32 60 67 44 77 24 69 79 38 66 74 75 62 75 79 79 46

24 96 420 12 24 36 72 36 108 72 60 96 36 1 60 24 12 1 1 2 7 2 1 1 1 1 1

Type of lesion

Location of lesion

Walking aid

Sporadic cerebellar ataxia SCA (unknown etiology) Sporadic cerebellar ataxia MSAC MSAC Sporadic cerebellar ataxia Sporadic cerebellar ataxia Sporadic cerebellar ataxia Sporadic cerebellar ataxia SCA1 SCA1 Cerebello-pyramidal syndrome Alcoholic cerebellar degeneration Haemorragic Ischaemic Haemorragic Ischaemic Ischaemic Ischaemic Haemorragic Haemorragic Haemorragic Ischaemic Ischaemic Ischaemic Haemorragic Ischaemic

Cerebellar atrophy Brainstem atrophy Vermian atrophy Pontocerebellar athophy Cerebellar atrophy Cerebellar atrophy Vermian atrophy Hemispheric and vermian atrophy Cerebellar atrophy Cerebellar atrophy Hemispheric and vermian atrophy Cortical cerebellar atrophy Hemispheric and vermian atrophy L cerebellar hemisphere L cerebellar hemisphere R cerebellar hemisphere Bilateral cerebellar hemisphere (L > R) Bilateral cerebellar hemisphere (L > R) R cerebellar hemisphere and R side of medulla L cerebellar hemisphere and vermis Vermis R cerebellar hemisphere R cerebellar hemisphere R cerebellar hemisphere R cerebellar hemisphere L cerebellar hemisphere L cerebellar hemisphere

Walker Cane Walker Walker No No Walker No No No No No Cane No No Walker Cane Cane No No Walker Walker Walker Walker Cane Cane Walker

M, male; F, female; SCA, spinocerebellar ataxia; MSAC, Multiple System Atrophy with predominance of cerebellar ataxia; R, right, L, left. Table 2 Mean values of balance and gait variables at baseline in the two groups of patients Degenerative Sway Area EO (mm2 ) SE Sway Area EC (mm2 ) SE Berg Balance Scale Range Velocity (cm/sec) SE Stride length (cm) SE Cadence (steps/min) SE Step width (cm) SE SARA Range FIM Range

467.1 69.2 927.5 158.3 32.1 15–46 63.9 9.4 78.6 9.2 97.6 7.2 14.8 0.9 17.9 9.0–25.5 109.7 93–123

Vascular

Student’s t-test

Mann-Whitney’s U-test

511.8 95.2 1026.8 240.3 28.3 15–49 59.1 10.4 75.2 8.6 89.0 7.1 12.0 0.9 12.9 8.5–20 88.6 53–112

0.71



0.73





0.26

0.73



0.79



0.41



0.05





0.002



0.001

SARA, Scale for the Assessment and Rating of Ataxia; FIM, Functional Independence Measure; SE, standard error.

and with eyes closed (EC). The feet were placed at an angle of ± 15◦ from the sagittal plane and the distance between the heels was 2 cm. Two 51 s-trials for

each visual condition were performed. The forces acting on the platform were sampled at 5 Hz, according to published norms (Gagey et al., 1988). A program

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calculated the sway area (the 95% confidence ellipse of the dispersion of center of pressure, CoP). This measure has been shown to be reliable, valid and responsive to changes in balance impairment (Pinsault and Vuillerme, 2009; Nardone and Schieppati, 2010). For each subject, the data of the two stance trials recorded for each visual condition were averaged prior to statistical analysis. 2.3.2. Baropodometry Gait was recorded and analyzed through a 4 msensorized walkway (GAITRite®, CIR Systems, Inc. 376 Lafayette Ave, Suite 202 Sparta, NJ 07871, USA) (Chien et al., 2006). This device produces reliable measurements of gait parameters that have been used to evaluate the effects of various interventions on walking speed, cadence and step length (Titianova et al., 2004; Menz et al., 2004; Webster et al., 2005). Patients began walking EO 2 m ahead of the mat and continued walking 2 m past the end at their usual velocity. Before data collection, participants practiced one walking trial in order to familiarize with the procedure. Then, all patients performed four successive trials in sequence (rest periods were allowed). Velocity, step length, cadence, step width were averaged over the four trials for further analysis. These variables represent relevant temporal and spatial measures of gait, already examined in previous studies of cerebellar disease (Ilg et al., 2007; Morton et al., 2010; Stolze et al., 2002). 2.3.3. Functional Evaluations At admission, ataxia was scored from 0 (no ataxia) to 40 (most severe) according to the scale for the assessment and rating of ataxia (SARA) (Schmitz-Hubsch et al., 2006) which is a valid measure of disease severity in several cerebellar diseases (B¨urk et al., 2009; Weyer et al., 2007). Before and after treatment, balance impairment was measured by using the Berg Balance Scale (BBS) (Berg et al., 1992; Bogle and Newton, 1996; Blum et al., 2008), that consists of 14 items, each scoring 0 to 4 (4 = normal), with a total score of 56. Disability was measured by trained physical therapists using the motor and cognitive components of the Functional Independence Measure (FIM) (Kidd et al., 1995). Independence was scored on a 18-item scale from 7 (‘totally independent’) to 1 (‘totally dependent’ or ‘not testable’), with a total score of 126. The assessors of all evaluations were blinded as to which group the patients belonged to.

2.4. Statistical analysis In the Figures, the upper or lower normal limits for stabilometry (Gagey et al., 1988) and baropodometry (Hollman et al., 2011; Menz et al., 2004), respectively, are indicated (mean and 2 SDs). In the case of stabilometry, sway area was compared by 3-way ANOVA between groups (degenerative, vascular) as independent factors and within two repeated measures (pre-post treatment, EO and EC). In the case of baropodometry, data from the left and right step were averaged, since preliminary statistical comparison of the variables pertaining to the two legs produced no significant difference. Each spatial-temporal variable was compared by 2-way ANOVA between groups (degenerative, vascular) as independent factors, and within repeated measures (pre-post treatment). The NewmanKeuls test was used for post-hoc comparisons. When using ordinal scales, as in the case of BBS, FIM and SARA, the Mann-Whitney U-test and Wilcoxon test were used, respectively, for unpaired (between groups) and paired comparisons (before vs after treatment). The standardized mean difference (SMD) assessed the magnitude of improvement between patients with degenerative and vascular ataxia. SMD allowed to directly comparing the effects of treatment on variables of different nature. SMD values larger than 0.2 represent small differences, around 0.5 moderate differences, and 0.8 or greater large differences (Cohen, 1988). For all analyses, statistical softwares (Statistica, StatSoft Inc, 2300 E 14th St, Tulsa, OK 74104, USA; MedCalc, Broekstraat 52, 8030 Mariakerke, Belgium) were used.

3. Results Age, gender, time since onset of disease, type and location of lesion, and use of walking aids are presented in Table 1. There were no differences in age (P = 0.30, unpaired t-test) or gender (P = 0.17, chi-squared test) between the vascular and degenerative group. Time since onset was 84.0 months ± 105.6 (SD) and 8.3 months ± 16.2, for degenerative and vascular group, respectively (P = 0.01, unpaired t-test). 3.1. Postural stability during quiet stance Figure 1 (upper panel) shows the values of sway area EO and EC of each patient of the degenerative and

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Fig. 1. Upper panel. Values of sway area with eyes open and eyes closed obtained from each patient of the degenerative and vascular group before and after treatment. Numbers and letters identify single degenerative and vascular patients, respectively, as in Table 1. Left and right graphs refer to the eyes-open and eyes-closed condition, respectively (note the different range of the ordinates). In both patient groups, there was a large inter-subject variability and moderate changes after treatment. Lower panel. Mean body sway area (+standard error, SE) during quite stance before and after treatment in the degenerative and vascular patient group. Horizontal dotted lines in the graphs correspond to the upper normal limits (mean + 2 SDs). Table 3 Physical therapy effects on balance and gait in cerebellar dysfunctions of vascular or degenerative origin Stabilometry Sway Area (mm2 )

Gait Velocity (cm/sec)

Cadence (steps/min)

Step width (cm)

ANOVA F

df

V vs D EO vs EC After vs before Interaction

0.00 22.06 9.34 1.59

1,24 1,24 1,24 1,24

P 0.99

Effects of balance and gait rehabilitation in cerebellar disease of vascular or degenerative origin.

To investigate whether the response to rehabilitation differs between patients with abnormalities of balance and gait due to vascular or to degenerati...
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