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ScienceDirect www.sciencedirect.com Annals of Physical and Rehabilitation Medicine 57 (2014) 570–577
Original article / Article original
Does galvanic vestibular stimulation reduce spatial neglect? A negative study Diminution de la ne´gligence spatiale unilate´rale par stimulation galvanique vestibulaire ? Une e´tude ne´gative A. Ruet a,*,b, C. Jokic c, P. Denise d,e, F. Leroy d,f, P. Azouvi a,b a
Service de me´decine physique et de re´adaptation, hoˆpital Raymond-Poincare´, AP–HP, 104, boulevard Raymond-Poincare´, 92380 Garches, France b Universite´ de Versailles Saint-Quentin-en-Yvelines, EA4497, 55, avenue de Paris, 78000 Versailles, France c Service de me´decine physique et de re´adaptation, hoˆpital Louis-Lacaine, 5, rue de l’Hoˆpital, 14260 Aunay-sur-Odon, France d Universite´ de Normandie, avenue de la Coˆte-de-Nacre, 14000 Caen, France e Inserm, U 1075 COMETE, avenue de la Coˆte-de-Nacre, 14032 Caen, France f Service de me´decine physique et de re´adaptation, CHU de Caen, avenue de la Coˆte-de-Nacre, 14032 Caen, France Received 14 March 2013; accepted 21 September 2014
Abstract Introduction. – In spatial neglect, the functional benefit of rehabilitation methods is subject to debate. A few studies have reported that galvanic vestibular stimulation (GVS) is efficacious in spatial neglect. The objective of the present study was to establish whether the effects of GVS persist after the end of stimulation. Materials. – Four patients with pathological rightward deviation in a bisection task at least three months after right hemisphere stroke. A singleblind, randomized crossover design was used to assess the effects of GVS on performance in line bisection and star cancellation tasks under three different conditions (cathode-right, cathode-left and sham stimulation). Results. – There were no significant differences in the performance of either task following GVS (relative to sham stimulation). Conclusion. – Galvanic vestibular stimulation did not reduce spatial neglect symptoms in any of the stimulation conditions. Further studies are necessary to understand the disparity between our results and those reported in the literature. Repeated sessions, a higher current intensity and/or alternating-current stimulation may improve this method before it can be used clinically. # 2014 Elsevier Masson SAS. All rights reserved. Keywords: Spatial neglect; Galvanic vestibular stimulation
Re´sume´ Introduction. – L’inte´reˆt fonctionnel des techniques de re´e´ducation de la ne´gligence spatiale unilate´rale (NSU) est discute´. Quelques e´tudes rapportent un effet de la stimulation galvanique vestibulaire (SGV) pour traiter la NSU. Nous cherchons a` de´terminer si l’effet de la SGV persiste a` l’arreˆt des stimulations. Patients et me´thode. – Cette e´tude inclus 4 patients a` 3 mois minimum d’un AVC de l’he´misphe`re droit pre´sentant une de´viation pathologique sur l’e´preuve de bissection de lignes de 20 cm. L’effet de la SGV et sa dure´e sont e´tudie´s dans un sche´ma d’e´tude croise´ dans diffe´rentes conditions (cathode a` gauche, cathode a` droite et simule´e) et sur deux e´preuves : bissection de lignes et barrage de cibles. Re´sultats. – Les re´sultats obtenus sous SGV, quel qu’en soit le sens (cathode a` droite–anode a` gauche ou inverse), ne sont pas diffe´rents de ceux obtenus sous condition simule´e.
* Corresponding author. E-mail addresses: [email protected], [email protected] (A. Ruet). http://dx.doi.org/10.1016/j.rehab.2014.09.009 1877-0657/# 2014 Elsevier Masson SAS. All rights reserved.
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Conclusion. – Nous ne retrouvons pas d’effet significatif de la SGV quel que soit le sens de stimulation. Des e´tudes supple´mentaires sont ne´cessaires pour comprendre les divergences avec les re´sultats de´ja` de´crits. Les effets de se´ances de re´pe´te´es, d’une SGV de plus forte intensite´ ou d’un courant alternatif pourraient ame´liorer cette technique avant d’envisager son utilisation en re´e´ducation. # 2014 Elsevier Masson SAS. Tous droits re´serve´s. Mots cle´s : Accident vasculaire ce´re´bral ; Ne´gligence spatiale unilate´rale ; Stimulation galvanique vestibulaire
1. English version 1.1. Introduction Unilateral spatial neglect (USN) syndrome is conventionally defined as an inability to detect, move towards, or respond to significant stimuli delivered contralaterally to a brain lesion and that cannot be attributed to sensorimotor impairment [1]. Unilateral spatial neglect occurs in 25 to 30% of stroke victims [2] and is predictive of a poor functional outcome [3–5]. Furthermore, USN appears to have a negative impact on poststroke quality of life [6,7]. Relief of the symptoms of USN is thus a major challenge on both individual and societal levels. In 2006, Luaute et al.’s literature review [8] identified 18 different rehabilitational approaches for left USN. The techniques’ respective degrees of efficacy are subject to debate [9]. A temporary decrease in USN symptoms has been described following the application of different types of sensory stimulation [10]. Caloric vestibular stimulation (CVS) consists in activation of the vestibular system via the instillation of warm or cold water into the external auditory meatus. This technique is associated with a reduction in neglect symptoms such as tactile neglect [11], representational disorders [12], somatoparaphrenia [13,14] and related symptoms such as anosognosia and hemiplegia [14]. Nevertheless, the use of CVS in rehabilitation is limited by practical aspects and its frequent side effects (nystagmus, nauseas and dizziness) [15]. Galvanic vestibular stimulation (GVS) consists in the activation of the vestibular system by application of direct current to the skin over the mastoids. In contrast to CVS, GVS is associated with very few adverse effects; several studies of small numbers of patients have suggested that GVS might be a valuable way of reducing the symptoms of USN [16–18]. Moreover, the ability to perform sham stimulation (analogous to a placebo [16]) enables statistical analysis of the GVS’s effects. The fact that GVS is simpler and less costly to implement than transcranial magnetic stimulation and CVS means that its use in rehabilitation can be envisaged. A decrease in visuospatial neglect during GVS [18–20] and a lasting reduction in tactile extinction after GVS (even some time after stroke) [21,22] have already been demonstrated. Left-cathodal GVS led to a decrease in deviation of the subjective vertical in patients with right hemisphere damage [9]. Left arm position sense (which can be altered by right-cathodal GVS in righthanded healthy subjects [23]) was improved by left-cathodal GVS in patients with left USN [24]. Line bisection is deviated leftwards by right-cathodal GVS in right-handed healthy subjects [25]. Case studies have described a reduction in
prosopagnosia and improvements in figure-copying during GVS [26,27]. Galvanic vestibular stimulation is cheap, easy to implement and can be applied to most patients (even soon after stroke). Improved left-side visual exploration during leftcathodal GVS has already been described in patients suffering from USN. The objective of the present study was to determine whether the improvement in the leftwards visual exploration persisted after the end of GVS. This duration will influence the value and efficacy of this type of treatment and the way the technique can be implemented as part of a rehabilitation programme. 1.2. Patients and methods In the present interventional, prospective, single-blind, crossover feasibility study, each patient was treated with three different GVS modes. Patients were recruited from the neurological rehabilitation clinics at Raymond Poincare´ University Hospital (Garches, France) and Aunay sur Odon General Hospital (Aunay sur Odon, France). The main inclusion criteria were the occurrence of a first right ischemic or hemorrhagic stroke more than 3 months previously (to diminish the effects of spontaneous recovery), and a 20 cm line bisection test result suggestive of left USN (i.e. a rightwards deviation of more than 6.5 mm). The exclusion criteria included the standard contra-indications to GVS (epilepsy, the presence of a pacemaker or intracranial ferromagnetic material, and skin damage over the mastoids), participation in another USN trial, corrected visual acuity that prevented closeup reading, vestibular damage and pre-existing neurological disease. Table 1 summarizes the characteristics of the study patients. The Catherine Bergego scale was used to assess USN behaviour in everyday life and it ranges from 0 (least severe) to 30 (most severe) [28,29]. All patients displayed homonymous hemianopsia and left proportional hemiplegia. Only one patient (KJ) had resumed walking, with the aid of a crutch. For each GVS condition, tests were performed before, during, immediately after and ten minutes after stimulation. The primary efficacy criterion was the deviation in the line bisection task (length: 20 cm; width: 1 mm) taken from the batterie d’e´valuation de la ne´gligence (BEN) battery [30]. Each line was presented on an A4 sheet placed horizontally in front of the patient. The patient had to mark the centre of the line with a pencil mark. The deviation (in mm) relative to the centre of the line was measured. By convention, rightward and leftward deviations were given positive and negative values, respectively. The baseline was measured for an average of 8 bisections (range: 5–9). On average, 4 bisections (range: 3–5) were
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572 Table 1 Characteristics of the patients. Patient
Gender
Age (years)
Handedness
Educational level/profession
Lesion sites
Time since stroke (months)
CBS score
Stimulation order
BP KJ CB FG
M M M M
61 38 66 69
Right-handed Right-handed Right-handed Right-handed
University degree/nurse Left school at 12/cook Left school at 16/company director University degree/decorator
Temporo-insular, deep frontal Frontoparietal, thalamic, CGN Frontoparietal, CGN Frontoparietal
3.5 12 3 3
22 20 16.25 22
RC-sham-LC Sham-RC-LC RC-LC-sham LC-sham-RC
CBS: the Catherine Bergego Scale, which measures the severity of USN in everyday life and ranges from 0 (least severe) to 30 (most severe). CGN: central grey nuclei. RC: right-cathodal, left-anodal GVS, LC: left-cathodal, right-anodal GVS, sham: sham stimulation.
have been informed of its procedures, its objectives and the risks associated with GVS. 1.3. Results The scores in the 20 cm line bisection test are summarized in Fig. 1 for each patient and each condition. There were no significant differences between the three stimulation conditions (P = 0.89 in the Friedman test). The mean total number of cancelled stars is not shown for the tests performed 10 min after the right-cathodal GVS or 10 min after the sham condition because these measurements were not performed in all patients (Fig. 2) and thus would not have been comparable with those recorded in the other conditions. None of the conditions was associated with a significant increase in the total number stars cancelled (P = 0.58 in the Friedman test). Patients FG and BP obtained better results in both tests during right-cathodal stimulation, as expected. At the end of each session, the patient was always asked to describe the sensations felt during the stimulation. Patient KJ reported a burning sensation under the right mastoid electrode in all stimulation modes, although it did not reach the pain threshold. Sham stimulation also produced this sensation, albeit less intensely. The patient had a scar from a decompressive craniectomy above the right mastoid and dysaesthesia in the 75 65 55 Deviaon in mm
performed at each measurement time point before, during and after GVS. The patients also performed the star cancellation test from the Behavioural Inattention Test (BIT) battery [31]. The efficacy criterion was the total number of small stars cancelled. In the star cancellation test, three omissions suggest the presence of an attentional disorder. This test was performed once before, during and after GVS. The order in which the various stimulation conditions were administered is given in Table 1. Galvanic vestibular stimulation was applied with a regulated, direct-current device (Galvadyn, Electronic Conseil, Gallargues Le Montueux, France) with a maximum output current of 20 mA and a maximum output voltage of 30 V. The carbon electrodes (4 cm 6 cm) were covered with a salinesoaked sponge held in place over the mastoids with a strap. Each patient was exposed to three different stimulation conditions: cathode-left anode-right, cathode-right anode-left, and sham stimulation. The time interval between the stimulations was always greater than 48 h, so that the results were not perturbed by a post-effect of previous stimulation. The patients were not informed about the type of stimulation delivered at each session. During stimulation, the current intensity was increased manually by 0.1 mA per second until a value of 1.5 mA was reached. During increases and decreases in current intensity, GVS can induce a slight itching sensation. Hence, during sham stimulation, the current was increased in the same way and then turned off after a few seconds. Sham stimulations were performed with the cathode on the left mastoid and the anode on the right mastoid, making it impossible for the patient to distinguish between real and sham stimulations [32]. In each condition, the stimulation lasted for 20 min. This duration was chosen in compliance with the safety guidelines on direct-current transcranial stimulation [33]. The tests were performed after 10 minutes of stimulation. A preset alarm signalled the end of the stimulation period and the stimulator switched itself off automatically. Statistical analyses of the data were performed with R software (version 2.14.1) [34]. The Friedman test was used to compare the mean deviations recorded with each type of stimulation. The Friedman test is a non-parametric test that can compare k-paired samples corresponding to k therapeutic conditions for the same blocks, in order to detect a difference between conditions. For the cancellation test, the Friedman test was also used to compare the total number of cancelled stars. In line with the tenets of the Declaration of Helsinki, all the patients gave their consent to participation in the study after
45
Paent BP
35
Paent CB
25
Paent FG
15
Paent KJ mean
5 -5
Fig. 1. Mean deviations in line bisection, for each patient and each stimulation condition. Base: baseline before the intervention; preRC: before right-cathodal, left-anodal GVS; RC: during RC; postRC: immediately after RC, postRC10: 10 min after RC; presham: before sham stimulation; sham: during sham stimulation; postsham: immediately after sham stimulation; postsham10: 10 min after sham stimulation; preLC: before left-cathodal, right-anodal GVS; LC: during LC; postLC: immediately after LC; postLC10: 10 min after LC.
A. Ruet et al. / Annals of Physical and Rehabilitation Medicine 57 (2014) 570–577
Number of stars cancelled
60 50 40 30 20 10
Pa
t BP
Pa
t CB
Pa
t FG
Pa
t KJ
mean
0
Fig. 2. Number of stars cancelled in the BIT star cancellation test, for each patient and each stimulation condition. Base: baseline before the intervention; preRC: before right-cathodal, left-anodal GVS; RC: during RC; postRC: immediately after RC, postRC10: 10 min after RC; presham: before sham stimulation; sham: during sham stimulation; postsham: immediately after sham stimulation; postsham10: 10 min after sham stimulation; preLC: before leftcathodal, right-anodal GVS; LC: during LC; postLC: immediately after LC; postLC10: 10 min after LC.
retroauricular region. The other patients had not felt any pain but did sometimes report an itching sensation under the electrode. No skin lesions under the electrodes were observed. 1.4. Discussion Galvanic vestibular stimulation did not significantly modify performance in the 20 cm line bisection test from the BEN and the star cancellation test from the BIT. These results do not confirm those of previous studies [19,20]. Utz et al. [20] used a variant of the Schenkenberg bisection test, featuring 17 lines for bisection on a sheet of paper. Only bisection of the lines situated furthest to the right on the sheet was significantly less deviated rightwards during GVS. The Schenkenberg test is perhaps more sensitive to variations in USN. Nevertheless, our results shown that GVS had no effect on the deviation in bisection of a single line placed in front of a patient suffering from left USN. In the star cancellation test, GVS was associated with a significant difference in the total number of stars cancelled. In the study by Rorsman et al. [19], GVS increased the number of cancelled targets in the BIT’s line crossing and star cancellation tests. Nevertheless, this improvement was not constant and GVS did not have a positive effect on the two tests at the same time, despite the larger number of patients in the study. In the study by Rorsman et al., infraliminal stimulation was delivered at an intensity of 0.7 to 1.7 mA (median: 1.15) only during performance of the tests [19]. In the present study, the stimulation method was exactly the same as that used by Utz et al. [20], and so does not explain the discordant results. In the absence of a significant effect, it is impossible to draw conclusions about the duration of this effect. In contrast, GVS is described in the literature as being simple to implement, cheap, and well tolerated. None of the patients complained about pain. The itching sensation felt under the electrode is a secondary effect that is frequently described in the literature.
573
Even though GVS is a relatively constraint-free technique, its efficacy is still subject to debate because our results contradict the literature data. Higher current intensities might have larger effects but might invalidate comparisons with sham stimulation. Increasing the number of stimulation sessions might conceivably constitute a way of increasing efficacy. However, a recent study showed that the improvement in performance in BIT tests was no greater after 10 sessions of GVS than after a single session [35]. In the absence of a placebo condition, the latter study of a large number of patients does not enable one to draw conclusions as to the effect of GVS. If GVS does have an effect on the symptoms of USN, the mechanism of action is poorly understood. The right posterior parietal cortex is active during bisection tasks, and damage to this region often induces USN [36–38]. During a bisection task in healthy subjects, functional MRI shows that GVS leads to greater activation of the ventral premotor cortex and posterior parietal cortex. Cortical activation in functional MRI experiments is greatest when direct-current GVS is turned on or turned off [39,40]. It would be interesting to study the effect of alternating current GVS on USN. It appears that cathode-right stimulation is associated with greater effects in visual exploration tasks [19,20]. The opposite configuration appears to have a greater effect on sensory extinction [21]. The stimulation modes might have different effects, depending on the patient and the type of lesion. The main limitation of the present study was the small number of patients. Moreover, only the patients were blinded to the type of stimulation applied. Use of the Schenkenberg Bisection Test would have enabled a more accurate comparison with the literature findings. To comply with safety rules, exposure to GVS did not exceed 20 minutes; this limited the number of tests that could be performed and the number of trials per test. Further research is required to better understand GVS’s mechanism of action and identify some effective stimulation modes. 1.5. Conclusion Relative to a sham condition, GVS did not decrease the symptoms of USN in line bisection and star cancellation tasks. Additional studies are needed to understand the divergences with the literature results. The effects of repeated sessions, higher-intensity GVS and alternating-current GVS should be studied, with a view to improving this technique before its use in rehabilitation can be considered. Disclosure of interest The authors have not supplied their declaration of conflict of interest. 2. Version franc¸aise 2.1. Introduction Le syndrome de ne´gligence spatiale unilate´rale (NSU) est classiquement de´fini comme l’incapacite´ de de´tecter, s’orienter
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vers, ou re´pondre a` des stimuli porteurs de signification situe´s du coˆte´ oppose´ a` une le´sion ce´re´brale et ne pouvant pas eˆtre attribue´e a` un de´ficit sensoriel ou moteur [1]. La ne´gligence spatiale unilate´rale, qui survient dans dans 25 a` 30 % des cas d’AVC [2], est un facteur de mauvais pronostic pour la re´cupe´ration fonctionnelle [3–5]. Elle semble avoir un impact ne´gatif sur la qualite´ de vie ressentie apre`s un AVC [6,7]. La re´duction des symptoˆmes de NSU repre´sente donc un enjeu majeur a` l’e´chelle individuelle et collective. Luaute´ et al. rapportent en 2006, dans une revue de la litte´rature [8], 18 diffe´rentes approches de re´e´ducation de la NSU gauche. L’efficacite´ des techniques propose´es est toujours discute´e [9]. Une diminution temporaire des symptoˆmes de NSU a e´te´ de´crite sous diffe´rents types de stimulations sensorielles [10]. La stimulation calorique vestibulaire (SCV) consiste en l’activation du syste`me vestibulaire par instillation d’eau chaude ou froide dans le conduit auditif externe. La SCV permet la re´duction des symptoˆmes de ne´gligence tels que la ne´gligence tactile [11], le trouble repre´sentationnel [12], la somatoparaphre´nie [13,14] ou de symptoˆmes associe´s comme l’anosognosie et l’he´miple´gie [14]. Ne´anmoins, l’utilisation de la SCV est limite´e en re´e´ducation par ses modalite´s de mise en œuvre et ses effets secondaires fre´quents (nystagmus, nause´es et vertiges) [15]. La stimulation galvanique vestibulaire (SGV) consiste en l’activation du syste`me vestibulaire par application d’un courant continu sur la peau en regard des mastoı¨des. Contrairement a` la SCV, la SGV n’entraıˆne quasiment pas d’effet inde´sirable et pourrait eˆtre un moyen inte´ressant de re´duire la NSU comme le sugge`rent plusieurs e´tudes d’effectifs limite´s [16–18]. De plus la possibilite´ d’effectuer une condition simule´e, e´quivalent a` un placebo [16], permet la mesure statistique des effets de cette stimulation. Elle est plus simple a` mettre en œuvre et moins couˆteuse que la stimulation magne´tique transcraˆnienne et la SCV, ce qui permet d’envisager son utilisation en re´e´ducation. Une diminution de la ne´gligence visuo-spatiale a de´ja` e´te´ de´montre´e pendant les stimulations [18–20], ainsi qu’une ame´lioration de l’extinction tactile durable meˆme a` distance de l’AVC [21,22]. La SGV cathodique gauche a permis une diminution de la de´viation de la verticale subjective apre`s le´sion he´misphe´rique droite [9]. Le sens de position du bras gauche qui peut eˆtre alte´re´ par la SGV cathodique droite chez des droitiers sains [23] est ame´liore´ par la SGV cathodique gauche en cas de NSU gauche [24]. La
bissection de ligne est de´vie´e vers la gauche sous SGV cathodique droite chez des droitiers sains [25]. Une diminution de la prosopagnosie et des ame´liorations en copie de figures sous SGV ont e´te´ de´crits dans des e´tudes de cas [26,27]. Cette technique peu couˆteuse, facile a` mettre en œuvre, peut eˆtre propose´e a` la majorite´ des patients meˆme rapidement apre`s la survenue d’un AVC. Une ame´lioration de l’exploration visuelle a` gauche a de´ja` e´te´ de´crite pendant la SGV chez des patients souffrant de NSU. Cette e´tude cherche a` de´terminer si l’ame´lioration de l’exploration visuelle vers la gauche se maintient a` l’arreˆt de la SGV. Cette dure´e conditionne l’inte´reˆt et l’efficacite´ d’une the´rapie et permet d’adapter la fac¸on dont cette technique peut eˆtre propose´e dans un programme de re´e´ducation. 2.2. Patients et me´thode Dans cette e´tude de faisabilite´, interventionnelle, prospective, en simple insu et de type croise´, trois modes de SGV ont e´te´ re´alise´s pour chaque patient. Les patients ont e´te´ recrute´s en re´e´ducation neurologique a` l’hoˆpital Raymond Poincare´ de Garches et au centre hospitalier d’Aunay sur Odon. Les crite`res d’inclusion e´taient la survenue d’un premier AVC droit ische´mique ou he´morragique datant de 3 mois au minimum (pour diminuer les effets de la re´cupe´ration spontane´e), une bissection de ligne de 20 cm en faveur d’une NSU gauche (par exemple de´viation de plus de 6,5 mm vers la droite). Les crite`res d’exclusion comprenaient les contre-indications a` la SGV (e´pilepsie, mate´riel ferro-magne´tique intracraˆnien, le´sion cutane´e en regard des mastoı¨des, pacemaker), la participation a` un autre protocole sur la NSU, une acuite´ visuelle corrige´e ne permettant pas la lecture de pre`s, une le´sion vestibulaire, une maladie neurologique pre´existante. Le Tableau 1 re´sume les caracte´ristiques des patients inclus. La ne´gligence spatiale en vie quotidienne a e´te´ e´value´e par l’e´chelle de Catherine Bergego allant de 0 a` 30 et sur laquelle le score augmente avec la se´ve´rite´ de la ne´gligence spatiale [28,29]. Tous les patients pre´sentaient une he´mianopsie late´rale homonyme et une he´miple´gie gauche proportionnelle. Seul le patient KJ avait repris la marche, avec une canne anglaise. Pour chaque condition, les tests ont e´te´ re´alise´s avant, pendant, imme´diatement apre`s puis 10 minutes apre`s la stimulation. Le crite`re principal mesure´ e´tait la de´viation des bissection de lignes de 20 cm de longueur et e´paisses d’1 mm
Tableau 1 Caracte´ristiques des patients. Patients
Sexe
ˆ ge A (ans)
Late´ralite´
Niveau d’e´tude/Profession
Localisation la le´sion
De´lai depuis l’AVC (mois)
Score ECB
Ordre des stimulations
BP KJ CB FG
M M M M
61 38 66 69
Droitier Droitier Droitier Droitier
BAC + 3/infirmier Scolarise´ jusqu’a` 12 ans/cuisinier CAP/directeur d’entreprise BAC + 3/de´corateur
Temporo-insulaire, Frontale profonde Fronto-parie´tale, Thalamique, NGC Fronto-parie´tale, NGC Fronto-parie´tale
3,5 12 3 3
22 20 16,25 22
RC-Sham-LC Sham-RC-LC RC-LC-Sham LC-Sham-RC
Score ECB : score sur l’e´chelle de Catherine Bergego en he´te´roe´valuation. L’e´chelle va de 0 a` 30, le maximum correspondant aux tableaux cliniques les plus se´ve`res de NSU. BAC + 3 : trois anne´es d’e´tudes apre`s le Baccalaure´at, CAP : Certificat d’aptitudes professionnelle ; NGC : noyaux gris centraux ; RC : SGV cathode a` droite et anode a` gauche ; LC : SGV cathode a` gauche et anode a` droite ; Sham : stimulation simule´e.
A. Ruet et al. / Annals of Physical and Rehabilitation Medicine 57 (2014) 570–577
2.3. Re´sultats Les scores au test de bissection de lignes de 20 cm sont reporte´s sur la Fig. 1 pour chaque patient et chaque condition. Aucune diffe´rence significative n’est mise en e´vidence entre les diffe´rentes conditions (test de Friedman, p = 0,89). Les moyennes du total d’e´toiles barre´es n’ont pas e´te´ repre´sente´es pour les tests effectue´s 10 min apre`s la condition cathode a` droite et 10 min apre`s la condition simule´e puisque ces mesures n’ont pas e´te´ faites chez tous les patients (Fig. 2). Elles n’auraient pas e´te´ comparables a` celles des autres conditions. Aucune des conditions n’ame´liore significativement le nombre total d’e´toiles barre´es (test de Friedman, p = 0,58). 75 65
Déviaon en mm
55 45
Paent BP
35
Paent CB
25
Paent FG
15
Paent KJ moyenne
5 -5
Fig. 1. De´viations moyennes en bissection de lignes par patient pour chaque condition de stimulation. Base : ligne de base avant intervention ; preRC : avant la SGV cathode a` droite et anode a` gauche ; RC : pendant RC ; postRC : imme´diatement apre`s RC, postRC10 : 10 min apre`s RC ; presham : avant la stimulation simule´e ; sham : pendant la stimulation simule´e ; postsham : imme´diatement apre`s sham ; postsham10 : 10 min apre`s sham ; preLC : avant la SGV cathode a` gauche anode a` droite ; LC : pendant LC ; postLC : imme´diatement apre`s LC ; postLC10 : 10 min apre`s LC. 60 50 nombre d'étoiles barrées
tire´es de la batterie d’e´valuation de la ne´gligence (BEN) [30]. Chaque ligne e´tait pre´sente´e sur une feuille A4 dispose´e horizontalement en face du patient. Le patient devait marquer le centre de la ligne d’un trait de crayon. La de´viation en millime`tre par rapport au centre de la ligne e´tait mesure´e. Par convention les de´viations vers la droite e´taient note´es positivement, celles vers la gauche ne´gativement. La ligne de base a e´te´ mesure´e sur 8 bissections en moyenne (min 5, max 9) et en moyenne 4 bissections (min 3, max 5) ont e´te´ re´alise´es a` chaque temps de mesure avant, durant et apre`s les SGV. Les patients ont e´galement passe´ l’e´preuve de barrage d’e´toiles de la batterie « Behavioral Inattention Test » [31]. Le crite`re e´value´ e´tait le nombre total de petites e´toiles barre´es. Dans ce test, trois omissions signent un trouble attentionnel. Ce test n’e´tait passe´ qu’une fois avant, durant et apre`s les SGV. L’ordre d’administration des diffe´rentes stimulations est indique´ dans le Tableau 1. L’appareil utilise´ pour la SGV e´tait un ge´ne´rateur de courant continu re´gule´ (Galvadyn, Electronic Conseil, Gallargues Le Montueux, France ; courant de sortie : 20 mA max ; tension de sortie : 30 V max). Les e´lectrodes de carbone (4 cm 6 cm) e´taient recouvertes d’une e´ponge imbibe´e de se´rum physiologique et maintenues en place sur les mastoı¨des par un bandeau. Chaque patient a rec¸u 3 conditions de stimulation : cathode a` gauche–anode a` droite, la condition inverse et une stimulation simule´e. L’e´cart entre les stimulations e´tait d’au minimum 48 h pour e´viter que les re´sultats ne soient perturbe´s par un post-effet de la stimulation pre´ce´dente. Les patients n’e´taient pas informe´s du type de stimulation rec¸u au cours de chaque se´ance. Au cours des stimulations, l’intensite´ e´tait augmente´e manuellement de 0,1 mA par seconde jusqu’a` 1,5 mA. Lors de l’augmentation et de la diminution d’intensite´, la SGV peut entraıˆner une le´ge`re de´mangeaison. Pour cette raison, lors de la stimulation simule´e le courant e´tait augmente´ de la meˆme manie`re puis arreˆte´ apre`s quelques secondes. Les stimulations simule´es ont e´te´ effectue´es cathode sur la mastoı¨de gauche et anode sur la droite. De cette manie`re la distinction entre les stimulations re´elles et simule´es est impossible [32]. La stimulation durait 20 min pour chaque condition. Cette dure´e a e´te´ choisie en accord avec les crite`res de se´curite´ propose´s pour la stimulation transcraˆnienne par courant direct [33]. Les tests e´taient re´alise´s apre`s 10 minutes de stimulation. Une alarme pre´re´gle´e sonnait la fin de la stimulation et le stimulateur s’e´teignait automatiquement. L’analyse statistique des donne´es a e´te´ re´alise´e a` l’aide du logiciel R version 2.14.1 [34]. Le test de Friedman a e´te´ utilise´ pour la comparaison des moyennes des de´viations mesure´es pour chaque type de stimulation. Le test de Friedman est non parame´trique et permet de comparer k e´chantillons appareille´s correspondant a` k conditions the´rapeutiques portants sur les meˆmes blocs, afin de mettre en e´vidence une diffe´rence entre les conditions. Pour l’e´preuve de barrage, le test de Friedman a e´galement e´te´ utilise´ pour comparer le nombre total d’e´toiles barre´es. Tous les patients ont donne´ leur accord pour participer a` l’e´tude apre`s avoir e´te´ informe´ de son de´roulement, de ses objectifs et des risques lie´s a` la SGV, en accord avec la de´claration d’Helsinki.
575
40 Paent BP 30 20 10
Paent CB Paent FG Paent KJ moyenne
0
Fig. 2. Nombre d’e´toiles barre´es par patient pour chaque condition sur l’e´preuve de barrage d’e´toile du Behavioural Inattention Test. Base : ligne de base avant intervention ; preRC : avant la SGV cathode a` droite et anode a` gauche ; RC : pendant RC ; postRC : imme´diatement apre`s RC, postRC10 : 10 min apre`s RC ; presham : avant la stimulation simule´e ; sham : pendant la stimulation simule´e ; postsham : imme´diatement apre`s sham ; postsham10 : 10 min apre`s sham ; preLC : avant la SGV cathode a` gauche anode a` droite ; LC : pendant LC ; postLC : imme´diatement apre`s LC ; postLC10 : 10 min apre`s LC.
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Les patients FG et BP ont obtenu de meilleurs re´sultats aux deux tests lors de la stimulation cathode a` droite comme nous l’avions attendu. Les patients ont e´te´ syste´matiquement interroge´s sur les sensations ressenties lors des stimulations a` la fin de chaque se´ance. Le patient KJ a rapporte´ des sensations de bruˆlures sous l’e´lectrode mastoı¨dienne droite quel que soit le mode de stimulation mais sans que cela n’atteigne le seuil douloureux. La stimulation factice produisait e´galement cette sensation mais de fac¸on moins intense. Le patient avait une cicatrice de craniectomie de´compressive au-dessus de la mastoı¨de droite et des dysesthe´sies dans la re´gion re´tro-auriculaire. Les autres patients n’ont pas ressenti de douleur mais parfois une sensation de de´mangeaison sous l’e´lectrode. Aucune le´sion cutane´e n’a e´te´ observe´e sous les e´lectrodes. 2.4. Discussion La stimulation galvanique vestibulaire de modifiait pas significativement les re´sultats aux tests de bissection de ligne de 20 cm de la BEN et de barrage d’e´toiles du Behavioral Inattention Test (BIT). Les re´sultats ne confirment pas les travaux ante´rieurs [19,20]. Dans l’e´tude de Utz et al. [20], une variante du test de bissection de Schenkenberg e´tait propose´e comprenant 17 lignes a` barrer sur une feuille. Seules les bissections des lignes situe´es les plus a` droite sur la feuille e´taient significativement moins de´vie´es a` droite sous SGV. Le test de Schenkenberg est possiblement plus sensible aux variations de la NSU. Ne´anmoins, nos re´sultats ont montre´ que la SGV n’avait pas d’effet sur la de´viation en bissection d’une ligne unique place´e face au patient souffrant de ne´gligence gauche. Pour l’e´preuve de barrage, la SGV ne modifiait pas significativement le nombre total d’e´toiles barre´es. Dans l’e´tude de Rorsman et al. [19], la SGV avait permis d’augmenter le nombre de cibles barre´es sur les e´preuves de barrage de lignes et d’e´toiles du BIT. Ne´anmoins, cette ame´lioration e´tait inconstante et l’effet positif de la SGV n’e´tait pas affirmable sur les 2 tests en meˆme temps malgre´ un plus grand nombre de patients. Dans l’e´tude de Rorsman et al. une stimulation infraliminale ´etait propose´e avec une intensite´ de 0,7 a` 1,7 mA (me´diane : 1,15) uniquement pendant la re´alisation des tests [19]. Dans notre e´tude la me´thode de stimulation e´tait identique a` celle de Utz et al. [20] et n’explique donc pas la diffe´rence des re´sultats. En l’absence d’effet significatif, il est impossible de conclure sur la dure´e de cet effet. En revanche, comme de´crit dans la litte´rature, la SGV est simple en pratique, peu couˆteuse, bien tole´re´e. Aucun patient ne s’est plaint de douleurs et les sensations de de´mangeaisons sous l’e´lectrode sont un effet secondaire fre´quemment de´crit dans la litte´rature. Si la SGV est une technique peu contraignante, la question de son efficacite´ reste discutable nos re´sultats e´tant contradictoire avec ceux pre´ce´demment de´crit. Des intensite´s plus e´leve´es pourraient avoir des effets supe´rieurs mais risquent de rendre impossible la comparaison a` un placebo. Un autre moyen d’ame´liorer l’efficacite´ pourrait eˆtre d’augmenter le nombre de se´ances de stimulation. Cependant une e´tude re´cente a montre´ que l’ame´lioration des performances sur les tests du
BIT n’est pas plus importante apre`s 10 se´ances de SGV qu’apre`s une se´ance unique [35]. En l’absence de condition placebo, cette dernie`re e´tude portant sur un effectif large ne permet pas de conclure sur l’effet de la SGV. S’il existe, le me´canisme d’action de la SGV sur les symptoˆmes de NSU est mal e´lucide´. Le cortex parie´tal poste´rieur droit est active´ dans les taˆches de bissection et sa le´sion entraıˆne fre´quemment une NSU [36–38]. Lors d’une taˆche de bissection chez le sujet sain, la SGV entraıˆne une augmentation d’activation des cortex pre´moteur ventral et parie´tal poste´rieur droits en IRMf. L’activation corticale en IRMf est maximale sous SGV lors de la mise en marche et de l’arreˆt du courant continu [39,40]. L’effet sur la NSU d’une stimulation vestibulaire par courant alternatif serait inte´ressant a` e´tudier. Il semble que la stimulation cathode a` droite entraıˆne de meilleurs effets sur des taˆches d’exploration visuelle [19,20]. La configuration inverse paraıˆt plus efficace sur l’extinction sensitive [21]. Les modes de stimulation pourraient avoir des effets diffe´rents selon les patients et leur type de le´sions. La limite principale de cette e´tude est son faible effectif. De plus, seuls les patients e´taient aveugles au type de stimulation rec¸u. L’utilisation du test de bissection de Schenkenberg aurait permis une meilleure comparaison aux re´sultats de´ja` publie´s. Pour respecter les re`gles de se´curite´, l’exposition a` la SGV n’a pas exce´de´ 20 minutes ce qui limitait le nombre de test propose´ et le nombre d’essais par test. De nouvelles e´tudes sont ne´cessaires pour mieux comprendre le me´canisme d’action de la SGV et trouver des modalite´s de stimulation efficaces. 2.5. Conclusion La SGV ne diminuait pas la NSU sur des taˆches de bissection de ligne et de barrage en comparaison a` une condition simule´e dans notre e´tude. Des e´tudes supple´mentaires sont ne´cessaires pour comprendre les divergences avec les re´sultats de´ja` de´crits. Les effets de se´ances de re´pe´te´es, d’une SGV de plus forte intensite´ ou d’un courant alternatif me´riteraient d’eˆtre e´tudie´s pour ame´liorer cette technique avant d’envisager son utilisation en re´e´ducation. De´claration d’inte´reˆts Les auteurs n’ont pas transmis de de´claration de conflits d’inte´reˆts. References [1] Heilman KM, Valenstein E, Watson RT. Neglect and related disorders. Semin Neurol 2000;20:463–70. [2] Appelros P, Karlsson GM, Seiger A, Nydevik I. Neglect and anosognosia after first-ever stroke: incidence and relationship to disability. J Rehabil Med Off J UEMS Eur Board Phys Rehabil Med 2002;34:215–20. [3] Denes G, Semenza C, Stoppa E, Lis A. Unilateral spatial neglect and recovery from hemiplegia: a follow-up study. Brain 1982;105(Pt 3):543–52. [4] Jehkonen M, Ahonen JP, Dastidar P, Koivisto AM, Laippala P, Vilkki J, et al. Visual neglect as a predictor of functional outcome one year after stroke. Acta Neurol Scand 2000;101:195–201. [5] Paolucci S. The role of unilateral spatial neglect in rehabilitation of right brain[ndash]damaged ischemic stroke patients: a matched comparison. Arch Phys Med Rehabil 2001;82:743–9.
A. Ruet et al. / Annals of Physical and Rehabilitation Medicine 57 (2014) 570–577 [6] Franceschini M, La Porta F, Agosti M, Massucci M. Is healthrelated-quality of life of stroke patients influenced by neurological impairments at one year after stroke? Eur J Phys Rehabil Med 2010;46: 389–99. [7] Sturm JW, Donnan GA, Dewey HM, Macdonell RAL, Gilligan AK, Srikanth V, et al. Quality of life after stroke: the North East Melbourne Stroke Incidence Study (NEMESIS). Stroke 2004;35:2340–5. [8] Luaute´ J, Halligan P, Rode G, Rossetti Y, Boisson D. Visuo-spatial neglect: a systematic review of current interventions and their effectiveness. Neurosci Biobehav Rev 2006;30:961–82. [9] Saj A, Honore´ J, Rousseaux M. Perception of the vertical in patients with right hemispheric lesion: effect of galvanic vestibular stimulation. Neuropsychologia 2006;44:1509–12. [10] Chokron S, Dupierrix E, Tabert M, Bartolomeo P. Experimental remission of unilateral spatial neglect. Neuropsychologia 2007;45:3127–48. [11] Cappa S, Sterzi R, Vallar G, Bisiach E. Remission of hemineglect and anosognosia during vestibular stimulation. Neuropsychologia 1987;25: 775–82. [12] Rode G, Perenin MT. Temporary remission of representational hemineglect through vestibular stimulation. Neuroreport 1994;5:869–72. [13] Bisiach E, Rusconi ML, Vallar G. Remission of somatoparaphrenic delusion through vestibular stimulation, vol. 29. 1991. [14] Rode G, Charles N, Perenin MT, Vighetto A, Trillet M, Aimard G. Partial remission of hemiplegia and somatoparaphrenia through vestibular stimulation in a case of unilateral neglect, vol. 28. 1992. [15] Bottini G, Karnath HO, Vallar G, Sterzi R, Frith CD, Frackowiak RS, et al. Cerebral representations for egocentric space: functional-anatomical evidence from caloric vestibular stimulation and neck vibration. Brain 2001;124:1182–96. [16] Utz KS, Dimova V, Oppenla¨nder K, Kerkhoff G. Electrified minds: transcranial direct current stimulation (tDCS) and galvanic vestibular stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology – a review of current data and future implications. Neuropsychologia 2010;48:2789–810. [17] Utz KS, Korluss K, Schmidt L, Rosenthal A, Oppenla¨nder K, Keller I, et al. Minor adverse effects of galvanic vestibular stimulation in persons with stroke and healthy individuals. Brain Inj 2011;25:1058–69. [18] Zubko O, Wilkinson D, Langston D, Sakel M. The effect of repeated sessions of galvanic vestibular stimulation on target cancellation in visuospatial neglect: preliminary evidence from two cases. Brain Inj 2013; 27:613–9. [19] Rorsman I, Magnusson M, Johansson BB. Reduction of visuo-spatial neglect with vestibular galvanic stimulation. Scand J Rehabil Med 1999;31:117–24. [20] Utz KS, Keller I, Kardinal M, Kerkhoff G. Galvanic vestibular stimulation reduces the pathological rightward line bisection error in neglect-a sham stimulation-controlled study. Neuropsychologia 2011;49:1219–25. [21] Kerkhoff G, Hildebrandt H, Reinhart S, Kardinal M, Dimova V, Utz KS. A long-lasting improvement of tactile extinction after galvanic vestibular stimulation: two Sham-stimulation controlled case studies. Neuropsychologia 2011;49:186–95. [22] Schmidt L, Utz KS, Depper L, Adams M, Schaadt A-K, Reinhart S, et al. Now you feel both: galvanic vestibular stimulation induces lasting improvements in the rehabilitation of chronic tactile extinction. Front Hum Neurosci 2013;7:90.
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[23] Schmidt L, Artinger F, Stumpf O, Kerkhoff G. Differential effects of galvanic vestibular stimulation on arm position sense in right- vs. lefthanders. Neuropsychologia 2013;51:893–9. [24] Schmidt L, Keller I, Utz KS, Artinger F, Stumpf O, Kerkhoff G. Galvanic vestibular stimulation improves arm position sense in spatial neglect: a sham-stimulation-controlled study. Neurorehabil Neural Repair n.d.;27: 497–506. [25] Ferre` ER, Day BL, Bottini G, Haggard P. How the vestibular system interacts with somatosensory perception: a sham-controlled study with galvanic vestibular stimulation. Neurosci Lett 2013. [26] Wilkinson D, Ko P, Kilduff P, McGlinchey R, Milberg W. Improvement of a face perception deficit via subsensory galvanic vestibular stimulation. J Int Neuropsychol Soc 2005;11:925–9. [27] Wilkinson D, Zubko O, Degutis J, Milberg W, Potter J. Improvement of a figure copying deficit during subsensory galvanic vestibular stimulation. J Neuropsychol 2010;4:107–18. [28] Azouvi P, Olivier S, de Montety G, Samuel C, Louis-Dreyfus A, Tesio L. Behavioral assessment of unilateral neglect: study of the psychometric properties of the Catherine Bergego Scale. Arch Phys Med Rehabil 2003;84:51–7. [29] Bergego C, Azouvi P, Samuel C, Marchal F, Louis-Dreyfus A, Jokic C, et al. Validation d’une e´chelle d’e´valuation fonctionnelle de l’he´mine´gligence dans la vie quotidienne : l’e´chelle CB. Ann Readapt Med Phys 1995;38:183–9. [30] Azouvi P, Bartolomeo P, Beis JM, Perennou D, Pradat-Diehl P, Rousseaux M. A battery of tests for the quantitative assessment of unilateral neglect. Restor Neurol Neurosci 2006;24:273–85. [31] Wilson B, Cockburn J, Halligan P. Development of a behavioral test of visuospatial neglect. Arch Phys Med Rehabil 1987;68:98–102. [32] Gandiga PC, Hummel FC, Cohen LG, Transcranial DC. stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin Neurophysiol Off J Int Fed Clin Neurophysiol 2006;117:845–50. [33] Nitsche MA, Liebetanz D, Antal A, Lang N, Tergau F, Paulus W. Modulation of cortical excitability by weak direct current stimulation – technical, safety and functional aspects. Suppl Clin Neurophysiol 2003;56:255–76. [34] Logiciel R http://www.r-project.org. [35] Wilkinson D, Zubko O, Sakel M, Coulton S, Higgins T, Pullicino P. Galvanic vestibular stimulation in hemi-spatial neglect. Front Integr Neurosci 2014;8:4. [36] Foxe JJ, McCourt ME, Javitt DC. Right hemisphere control of visuospatial attention: line-bisection judgments evaluated with high-density electrical mapping and source analysis. Neuroimage 2003;19:710–26. [37] Mort DJ, Malhotra P, Mannan SK, Rorden C, Pambakian A, Kennard C, et al. The anatomy of visual neglect. Brain 2003;126:1986–97. [38] Vallar G, Rusconi ML, Bignamini L, Geminiani G, Perani D. Anatomical correlates of visual and tactile extinction in humans: a clinical CT scan study. J Neurol Neurosurg Psychiatry 1994;57:464–70. [39] Stephan T, Deutschla¨nder A, Nolte A, Schneider E, Wiesmann M, Brandt T, et al. Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage 2005;26:721–32. [40] Stephan T, Hu¨fner K, Brandt T. Stimulus profile and modeling of continuous galvanic vestibular stimulation in functional magnetic resonance imaging. Ann N Y Acad Sci 2009;1164:472–5.
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Original article / Article original
Does galvanic vestibular stimulation reduce spatial neglect? A negative study Diminution de la ne´gligence spatiale unilate´rale par stimulation galvanique vestibulaire ? Une e´tude ne´gative A. Ruet a,*,b, C. Jokic c, P. Denise d,e, F. Leroy d,f, P. Azouvi a,b a
Service de me´decine physique et de re´adaptation, hoˆpital Raymond-Poincare´, AP–HP, 104, boulevard Raymond-Poincare´, 92380 Garches, France b Universite´ de Versailles Saint-Quentin-en-Yvelines, EA4497, 55, avenue de Paris, 78000 Versailles, France c Service de me´decine physique et de re´adaptation, hoˆpital Louis-Lacaine, 5, rue de l’Hoˆpital, 14260 Aunay-sur-Odon, France d Universite´ de Normandie, avenue de la Coˆte-de-Nacre, 14000 Caen, France e Inserm, U 1075 COMETE, avenue de la Coˆte-de-Nacre, 14032 Caen, France f Service de me´decine physique et de re´adaptation, CHU de Caen, avenue de la Coˆte-de-Nacre, 14032 Caen, France Received 14 March 2013; accepted 21 September 2014
Abstract Introduction. – In spatial neglect, the functional benefit of rehabilitation methods is subject to debate. A few studies have reported that galvanic vestibular stimulation (GVS) is efficacious in spatial neglect. The objective of the present study was to establish whether the effects of GVS persist after the end of stimulation. Materials. – Four patients with pathological rightward deviation in a bisection task at least three months after right hemisphere stroke. A singleblind, randomized crossover design was used to assess the effects of GVS on performance in line bisection and star cancellation tasks under three different conditions (cathode-right, cathode-left and sham stimulation). Results. – There were no significant differences in the performance of either task following GVS (relative to sham stimulation). Conclusion. – Galvanic vestibular stimulation did not reduce spatial neglect symptoms in any of the stimulation conditions. Further studies are necessary to understand the disparity between our results and those reported in the literature. Repeated sessions, a higher current intensity and/or alternating-current stimulation may improve this method before it can be used clinically. # 2014 Elsevier Masson SAS. All rights reserved. Keywords: Spatial neglect; Galvanic vestibular stimulation
Re´sume´ Introduction. – L’inte´reˆt fonctionnel des techniques de re´e´ducation de la ne´gligence spatiale unilate´rale (NSU) est discute´. Quelques e´tudes rapportent un effet de la stimulation galvanique vestibulaire (SGV) pour traiter la NSU. Nous cherchons a` de´terminer si l’effet de la SGV persiste a` l’arreˆt des stimulations. Patients et me´thode. – Cette e´tude inclus 4 patients a` 3 mois minimum d’un AVC de l’he´misphe`re droit pre´sentant une de´viation pathologique sur l’e´preuve de bissection de lignes de 20 cm. L’effet de la SGV et sa dure´e sont e´tudie´s dans un sche´ma d’e´tude croise´ dans diffe´rentes conditions (cathode a` gauche, cathode a` droite et simule´e) et sur deux e´preuves : bissection de lignes et barrage de cibles. Re´sultats. – Les re´sultats obtenus sous SGV, quel qu’en soit le sens (cathode a` droite–anode a` gauche ou inverse), ne sont pas diffe´rents de ceux obtenus sous condition simule´e.
* Corresponding author. E-mail addresses: [email protected], [email protected] (A. Ruet). http://dx.doi.org/10.1016/j.rehab.2014.09.009 1877-0657/# 2014 Elsevier Masson SAS. All rights reserved.
A. Ruet et al. / Annals of Physical and Rehabilitation Medicine 57 (2014) 570–577
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Conclusion. – Nous ne retrouvons pas d’effet significatif de la SGV quel que soit le sens de stimulation. Des e´tudes supple´mentaires sont ne´cessaires pour comprendre les divergences avec les re´sultats de´ja` de´crits. Les effets de se´ances de re´pe´te´es, d’une SGV de plus forte intensite´ ou d’un courant alternatif pourraient ame´liorer cette technique avant d’envisager son utilisation en re´e´ducation. # 2014 Elsevier Masson SAS. Tous droits re´serve´s. Mots cle´s : Accident vasculaire ce´re´bral ; Ne´gligence spatiale unilate´rale ; Stimulation galvanique vestibulaire
1. English version 1.1. Introduction Unilateral spatial neglect (USN) syndrome is conventionally defined as an inability to detect, move towards, or respond to significant stimuli delivered contralaterally to a brain lesion and that cannot be attributed to sensorimotor impairment [1]. Unilateral spatial neglect occurs in 25 to 30% of stroke victims [2] and is predictive of a poor functional outcome [3–5]. Furthermore, USN appears to have a negative impact on poststroke quality of life [6,7]. Relief of the symptoms of USN is thus a major challenge on both individual and societal levels. In 2006, Luaute et al.’s literature review [8] identified 18 different rehabilitational approaches for left USN. The techniques’ respective degrees of efficacy are subject to debate [9]. A temporary decrease in USN symptoms has been described following the application of different types of sensory stimulation [10]. Caloric vestibular stimulation (CVS) consists in activation of the vestibular system via the instillation of warm or cold water into the external auditory meatus. This technique is associated with a reduction in neglect symptoms such as tactile neglect [11], representational disorders [12], somatoparaphrenia [13,14] and related symptoms such as anosognosia and hemiplegia [14]. Nevertheless, the use of CVS in rehabilitation is limited by practical aspects and its frequent side effects (nystagmus, nauseas and dizziness) [15]. Galvanic vestibular stimulation (GVS) consists in the activation of the vestibular system by application of direct current to the skin over the mastoids. In contrast to CVS, GVS is associated with very few adverse effects; several studies of small numbers of patients have suggested that GVS might be a valuable way of reducing the symptoms of USN [16–18]. Moreover, the ability to perform sham stimulation (analogous to a placebo [16]) enables statistical analysis of the GVS’s effects. The fact that GVS is simpler and less costly to implement than transcranial magnetic stimulation and CVS means that its use in rehabilitation can be envisaged. A decrease in visuospatial neglect during GVS [18–20] and a lasting reduction in tactile extinction after GVS (even some time after stroke) [21,22] have already been demonstrated. Left-cathodal GVS led to a decrease in deviation of the subjective vertical in patients with right hemisphere damage [9]. Left arm position sense (which can be altered by right-cathodal GVS in righthanded healthy subjects [23]) was improved by left-cathodal GVS in patients with left USN [24]. Line bisection is deviated leftwards by right-cathodal GVS in right-handed healthy subjects [25]. Case studies have described a reduction in
prosopagnosia and improvements in figure-copying during GVS [26,27]. Galvanic vestibular stimulation is cheap, easy to implement and can be applied to most patients (even soon after stroke). Improved left-side visual exploration during leftcathodal GVS has already been described in patients suffering from USN. The objective of the present study was to determine whether the improvement in the leftwards visual exploration persisted after the end of GVS. This duration will influence the value and efficacy of this type of treatment and the way the technique can be implemented as part of a rehabilitation programme. 1.2. Patients and methods In the present interventional, prospective, single-blind, crossover feasibility study, each patient was treated with three different GVS modes. Patients were recruited from the neurological rehabilitation clinics at Raymond Poincare´ University Hospital (Garches, France) and Aunay sur Odon General Hospital (Aunay sur Odon, France). The main inclusion criteria were the occurrence of a first right ischemic or hemorrhagic stroke more than 3 months previously (to diminish the effects of spontaneous recovery), and a 20 cm line bisection test result suggestive of left USN (i.e. a rightwards deviation of more than 6.5 mm). The exclusion criteria included the standard contra-indications to GVS (epilepsy, the presence of a pacemaker or intracranial ferromagnetic material, and skin damage over the mastoids), participation in another USN trial, corrected visual acuity that prevented closeup reading, vestibular damage and pre-existing neurological disease. Table 1 summarizes the characteristics of the study patients. The Catherine Bergego scale was used to assess USN behaviour in everyday life and it ranges from 0 (least severe) to 30 (most severe) [28,29]. All patients displayed homonymous hemianopsia and left proportional hemiplegia. Only one patient (KJ) had resumed walking, with the aid of a crutch. For each GVS condition, tests were performed before, during, immediately after and ten minutes after stimulation. The primary efficacy criterion was the deviation in the line bisection task (length: 20 cm; width: 1 mm) taken from the batterie d’e´valuation de la ne´gligence (BEN) battery [30]. Each line was presented on an A4 sheet placed horizontally in front of the patient. The patient had to mark the centre of the line with a pencil mark. The deviation (in mm) relative to the centre of the line was measured. By convention, rightward and leftward deviations were given positive and negative values, respectively. The baseline was measured for an average of 8 bisections (range: 5–9). On average, 4 bisections (range: 3–5) were
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572 Table 1 Characteristics of the patients. Patient
Gender
Age (years)
Handedness
Educational level/profession
Lesion sites
Time since stroke (months)
CBS score
Stimulation order
BP KJ CB FG
M M M M
61 38 66 69
Right-handed Right-handed Right-handed Right-handed
University degree/nurse Left school at 12/cook Left school at 16/company director University degree/decorator
Temporo-insular, deep frontal Frontoparietal, thalamic, CGN Frontoparietal, CGN Frontoparietal
3.5 12 3 3
22 20 16.25 22
RC-sham-LC Sham-RC-LC RC-LC-sham LC-sham-RC
CBS: the Catherine Bergego Scale, which measures the severity of USN in everyday life and ranges from 0 (least severe) to 30 (most severe). CGN: central grey nuclei. RC: right-cathodal, left-anodal GVS, LC: left-cathodal, right-anodal GVS, sham: sham stimulation.
have been informed of its procedures, its objectives and the risks associated with GVS. 1.3. Results The scores in the 20 cm line bisection test are summarized in Fig. 1 for each patient and each condition. There were no significant differences between the three stimulation conditions (P = 0.89 in the Friedman test). The mean total number of cancelled stars is not shown for the tests performed 10 min after the right-cathodal GVS or 10 min after the sham condition because these measurements were not performed in all patients (Fig. 2) and thus would not have been comparable with those recorded in the other conditions. None of the conditions was associated with a significant increase in the total number stars cancelled (P = 0.58 in the Friedman test). Patients FG and BP obtained better results in both tests during right-cathodal stimulation, as expected. At the end of each session, the patient was always asked to describe the sensations felt during the stimulation. Patient KJ reported a burning sensation under the right mastoid electrode in all stimulation modes, although it did not reach the pain threshold. Sham stimulation also produced this sensation, albeit less intensely. The patient had a scar from a decompressive craniectomy above the right mastoid and dysaesthesia in the 75 65 55 Deviaon in mm
performed at each measurement time point before, during and after GVS. The patients also performed the star cancellation test from the Behavioural Inattention Test (BIT) battery [31]. The efficacy criterion was the total number of small stars cancelled. In the star cancellation test, three omissions suggest the presence of an attentional disorder. This test was performed once before, during and after GVS. The order in which the various stimulation conditions were administered is given in Table 1. Galvanic vestibular stimulation was applied with a regulated, direct-current device (Galvadyn, Electronic Conseil, Gallargues Le Montueux, France) with a maximum output current of 20 mA and a maximum output voltage of 30 V. The carbon electrodes (4 cm 6 cm) were covered with a salinesoaked sponge held in place over the mastoids with a strap. Each patient was exposed to three different stimulation conditions: cathode-left anode-right, cathode-right anode-left, and sham stimulation. The time interval between the stimulations was always greater than 48 h, so that the results were not perturbed by a post-effect of previous stimulation. The patients were not informed about the type of stimulation delivered at each session. During stimulation, the current intensity was increased manually by 0.1 mA per second until a value of 1.5 mA was reached. During increases and decreases in current intensity, GVS can induce a slight itching sensation. Hence, during sham stimulation, the current was increased in the same way and then turned off after a few seconds. Sham stimulations were performed with the cathode on the left mastoid and the anode on the right mastoid, making it impossible for the patient to distinguish between real and sham stimulations [32]. In each condition, the stimulation lasted for 20 min. This duration was chosen in compliance with the safety guidelines on direct-current transcranial stimulation [33]. The tests were performed after 10 minutes of stimulation. A preset alarm signalled the end of the stimulation period and the stimulator switched itself off automatically. Statistical analyses of the data were performed with R software (version 2.14.1) [34]. The Friedman test was used to compare the mean deviations recorded with each type of stimulation. The Friedman test is a non-parametric test that can compare k-paired samples corresponding to k therapeutic conditions for the same blocks, in order to detect a difference between conditions. For the cancellation test, the Friedman test was also used to compare the total number of cancelled stars. In line with the tenets of the Declaration of Helsinki, all the patients gave their consent to participation in the study after
45
Paent BP
35
Paent CB
25
Paent FG
15
Paent KJ mean
5 -5
Fig. 1. Mean deviations in line bisection, for each patient and each stimulation condition. Base: baseline before the intervention; preRC: before right-cathodal, left-anodal GVS; RC: during RC; postRC: immediately after RC, postRC10: 10 min after RC; presham: before sham stimulation; sham: during sham stimulation; postsham: immediately after sham stimulation; postsham10: 10 min after sham stimulation; preLC: before left-cathodal, right-anodal GVS; LC: during LC; postLC: immediately after LC; postLC10: 10 min after LC.
A. Ruet et al. / Annals of Physical and Rehabilitation Medicine 57 (2014) 570–577
Number of stars cancelled
60 50 40 30 20 10
Pa
t BP
Pa
t CB
Pa
t FG
Pa
t KJ
mean
0
Fig. 2. Number of stars cancelled in the BIT star cancellation test, for each patient and each stimulation condition. Base: baseline before the intervention; preRC: before right-cathodal, left-anodal GVS; RC: during RC; postRC: immediately after RC, postRC10: 10 min after RC; presham: before sham stimulation; sham: during sham stimulation; postsham: immediately after sham stimulation; postsham10: 10 min after sham stimulation; preLC: before leftcathodal, right-anodal GVS; LC: during LC; postLC: immediately after LC; postLC10: 10 min after LC.
retroauricular region. The other patients had not felt any pain but did sometimes report an itching sensation under the electrode. No skin lesions under the electrodes were observed. 1.4. Discussion Galvanic vestibular stimulation did not significantly modify performance in the 20 cm line bisection test from the BEN and the star cancellation test from the BIT. These results do not confirm those of previous studies [19,20]. Utz et al. [20] used a variant of the Schenkenberg bisection test, featuring 17 lines for bisection on a sheet of paper. Only bisection of the lines situated furthest to the right on the sheet was significantly less deviated rightwards during GVS. The Schenkenberg test is perhaps more sensitive to variations in USN. Nevertheless, our results shown that GVS had no effect on the deviation in bisection of a single line placed in front of a patient suffering from left USN. In the star cancellation test, GVS was associated with a significant difference in the total number of stars cancelled. In the study by Rorsman et al. [19], GVS increased the number of cancelled targets in the BIT’s line crossing and star cancellation tests. Nevertheless, this improvement was not constant and GVS did not have a positive effect on the two tests at the same time, despite the larger number of patients in the study. In the study by Rorsman et al., infraliminal stimulation was delivered at an intensity of 0.7 to 1.7 mA (median: 1.15) only during performance of the tests [19]. In the present study, the stimulation method was exactly the same as that used by Utz et al. [20], and so does not explain the discordant results. In the absence of a significant effect, it is impossible to draw conclusions about the duration of this effect. In contrast, GVS is described in the literature as being simple to implement, cheap, and well tolerated. None of the patients complained about pain. The itching sensation felt under the electrode is a secondary effect that is frequently described in the literature.
573
Even though GVS is a relatively constraint-free technique, its efficacy is still subject to debate because our results contradict the literature data. Higher current intensities might have larger effects but might invalidate comparisons with sham stimulation. Increasing the number of stimulation sessions might conceivably constitute a way of increasing efficacy. However, a recent study showed that the improvement in performance in BIT tests was no greater after 10 sessions of GVS than after a single session [35]. In the absence of a placebo condition, the latter study of a large number of patients does not enable one to draw conclusions as to the effect of GVS. If GVS does have an effect on the symptoms of USN, the mechanism of action is poorly understood. The right posterior parietal cortex is active during bisection tasks, and damage to this region often induces USN [36–38]. During a bisection task in healthy subjects, functional MRI shows that GVS leads to greater activation of the ventral premotor cortex and posterior parietal cortex. Cortical activation in functional MRI experiments is greatest when direct-current GVS is turned on or turned off [39,40]. It would be interesting to study the effect of alternating current GVS on USN. It appears that cathode-right stimulation is associated with greater effects in visual exploration tasks [19,20]. The opposite configuration appears to have a greater effect on sensory extinction [21]. The stimulation modes might have different effects, depending on the patient and the type of lesion. The main limitation of the present study was the small number of patients. Moreover, only the patients were blinded to the type of stimulation applied. Use of the Schenkenberg Bisection Test would have enabled a more accurate comparison with the literature findings. To comply with safety rules, exposure to GVS did not exceed 20 minutes; this limited the number of tests that could be performed and the number of trials per test. Further research is required to better understand GVS’s mechanism of action and identify some effective stimulation modes. 1.5. Conclusion Relative to a sham condition, GVS did not decrease the symptoms of USN in line bisection and star cancellation tasks. Additional studies are needed to understand the divergences with the literature results. The effects of repeated sessions, higher-intensity GVS and alternating-current GVS should be studied, with a view to improving this technique before its use in rehabilitation can be considered. Disclosure of interest The authors have not supplied their declaration of conflict of interest. 2. Version franc¸aise 2.1. Introduction Le syndrome de ne´gligence spatiale unilate´rale (NSU) est classiquement de´fini comme l’incapacite´ de de´tecter, s’orienter
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574
vers, ou re´pondre a` des stimuli porteurs de signification situe´s du coˆte´ oppose´ a` une le´sion ce´re´brale et ne pouvant pas eˆtre attribue´e a` un de´ficit sensoriel ou moteur [1]. La ne´gligence spatiale unilate´rale, qui survient dans dans 25 a` 30 % des cas d’AVC [2], est un facteur de mauvais pronostic pour la re´cupe´ration fonctionnelle [3–5]. Elle semble avoir un impact ne´gatif sur la qualite´ de vie ressentie apre`s un AVC [6,7]. La re´duction des symptoˆmes de NSU repre´sente donc un enjeu majeur a` l’e´chelle individuelle et collective. Luaute´ et al. rapportent en 2006, dans une revue de la litte´rature [8], 18 diffe´rentes approches de re´e´ducation de la NSU gauche. L’efficacite´ des techniques propose´es est toujours discute´e [9]. Une diminution temporaire des symptoˆmes de NSU a e´te´ de´crite sous diffe´rents types de stimulations sensorielles [10]. La stimulation calorique vestibulaire (SCV) consiste en l’activation du syste`me vestibulaire par instillation d’eau chaude ou froide dans le conduit auditif externe. La SCV permet la re´duction des symptoˆmes de ne´gligence tels que la ne´gligence tactile [11], le trouble repre´sentationnel [12], la somatoparaphre´nie [13,14] ou de symptoˆmes associe´s comme l’anosognosie et l’he´miple´gie [14]. Ne´anmoins, l’utilisation de la SCV est limite´e en re´e´ducation par ses modalite´s de mise en œuvre et ses effets secondaires fre´quents (nystagmus, nause´es et vertiges) [15]. La stimulation galvanique vestibulaire (SGV) consiste en l’activation du syste`me vestibulaire par application d’un courant continu sur la peau en regard des mastoı¨des. Contrairement a` la SCV, la SGV n’entraıˆne quasiment pas d’effet inde´sirable et pourrait eˆtre un moyen inte´ressant de re´duire la NSU comme le sugge`rent plusieurs e´tudes d’effectifs limite´s [16–18]. De plus la possibilite´ d’effectuer une condition simule´e, e´quivalent a` un placebo [16], permet la mesure statistique des effets de cette stimulation. Elle est plus simple a` mettre en œuvre et moins couˆteuse que la stimulation magne´tique transcraˆnienne et la SCV, ce qui permet d’envisager son utilisation en re´e´ducation. Une diminution de la ne´gligence visuo-spatiale a de´ja` e´te´ de´montre´e pendant les stimulations [18–20], ainsi qu’une ame´lioration de l’extinction tactile durable meˆme a` distance de l’AVC [21,22]. La SGV cathodique gauche a permis une diminution de la de´viation de la verticale subjective apre`s le´sion he´misphe´rique droite [9]. Le sens de position du bras gauche qui peut eˆtre alte´re´ par la SGV cathodique droite chez des droitiers sains [23] est ame´liore´ par la SGV cathodique gauche en cas de NSU gauche [24]. La
bissection de ligne est de´vie´e vers la gauche sous SGV cathodique droite chez des droitiers sains [25]. Une diminution de la prosopagnosie et des ame´liorations en copie de figures sous SGV ont e´te´ de´crits dans des e´tudes de cas [26,27]. Cette technique peu couˆteuse, facile a` mettre en œuvre, peut eˆtre propose´e a` la majorite´ des patients meˆme rapidement apre`s la survenue d’un AVC. Une ame´lioration de l’exploration visuelle a` gauche a de´ja` e´te´ de´crite pendant la SGV chez des patients souffrant de NSU. Cette e´tude cherche a` de´terminer si l’ame´lioration de l’exploration visuelle vers la gauche se maintient a` l’arreˆt de la SGV. Cette dure´e conditionne l’inte´reˆt et l’efficacite´ d’une the´rapie et permet d’adapter la fac¸on dont cette technique peut eˆtre propose´e dans un programme de re´e´ducation. 2.2. Patients et me´thode Dans cette e´tude de faisabilite´, interventionnelle, prospective, en simple insu et de type croise´, trois modes de SGV ont e´te´ re´alise´s pour chaque patient. Les patients ont e´te´ recrute´s en re´e´ducation neurologique a` l’hoˆpital Raymond Poincare´ de Garches et au centre hospitalier d’Aunay sur Odon. Les crite`res d’inclusion e´taient la survenue d’un premier AVC droit ische´mique ou he´morragique datant de 3 mois au minimum (pour diminuer les effets de la re´cupe´ration spontane´e), une bissection de ligne de 20 cm en faveur d’une NSU gauche (par exemple de´viation de plus de 6,5 mm vers la droite). Les crite`res d’exclusion comprenaient les contre-indications a` la SGV (e´pilepsie, mate´riel ferro-magne´tique intracraˆnien, le´sion cutane´e en regard des mastoı¨des, pacemaker), la participation a` un autre protocole sur la NSU, une acuite´ visuelle corrige´e ne permettant pas la lecture de pre`s, une le´sion vestibulaire, une maladie neurologique pre´existante. Le Tableau 1 re´sume les caracte´ristiques des patients inclus. La ne´gligence spatiale en vie quotidienne a e´te´ e´value´e par l’e´chelle de Catherine Bergego allant de 0 a` 30 et sur laquelle le score augmente avec la se´ve´rite´ de la ne´gligence spatiale [28,29]. Tous les patients pre´sentaient une he´mianopsie late´rale homonyme et une he´miple´gie gauche proportionnelle. Seul le patient KJ avait repris la marche, avec une canne anglaise. Pour chaque condition, les tests ont e´te´ re´alise´s avant, pendant, imme´diatement apre`s puis 10 minutes apre`s la stimulation. Le crite`re principal mesure´ e´tait la de´viation des bissection de lignes de 20 cm de longueur et e´paisses d’1 mm
Tableau 1 Caracte´ristiques des patients. Patients
Sexe
ˆ ge A (ans)
Late´ralite´
Niveau d’e´tude/Profession
Localisation la le´sion
De´lai depuis l’AVC (mois)
Score ECB
Ordre des stimulations
BP KJ CB FG
M M M M
61 38 66 69
Droitier Droitier Droitier Droitier
BAC + 3/infirmier Scolarise´ jusqu’a` 12 ans/cuisinier CAP/directeur d’entreprise BAC + 3/de´corateur
Temporo-insulaire, Frontale profonde Fronto-parie´tale, Thalamique, NGC Fronto-parie´tale, NGC Fronto-parie´tale
3,5 12 3 3
22 20 16,25 22
RC-Sham-LC Sham-RC-LC RC-LC-Sham LC-Sham-RC
Score ECB : score sur l’e´chelle de Catherine Bergego en he´te´roe´valuation. L’e´chelle va de 0 a` 30, le maximum correspondant aux tableaux cliniques les plus se´ve`res de NSU. BAC + 3 : trois anne´es d’e´tudes apre`s le Baccalaure´at, CAP : Certificat d’aptitudes professionnelle ; NGC : noyaux gris centraux ; RC : SGV cathode a` droite et anode a` gauche ; LC : SGV cathode a` gauche et anode a` droite ; Sham : stimulation simule´e.
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2.3. Re´sultats Les scores au test de bissection de lignes de 20 cm sont reporte´s sur la Fig. 1 pour chaque patient et chaque condition. Aucune diffe´rence significative n’est mise en e´vidence entre les diffe´rentes conditions (test de Friedman, p = 0,89). Les moyennes du total d’e´toiles barre´es n’ont pas e´te´ repre´sente´es pour les tests effectue´s 10 min apre`s la condition cathode a` droite et 10 min apre`s la condition simule´e puisque ces mesures n’ont pas e´te´ faites chez tous les patients (Fig. 2). Elles n’auraient pas e´te´ comparables a` celles des autres conditions. Aucune des conditions n’ame´liore significativement le nombre total d’e´toiles barre´es (test de Friedman, p = 0,58). 75 65
Déviaon en mm
55 45
Paent BP
35
Paent CB
25
Paent FG
15
Paent KJ moyenne
5 -5
Fig. 1. De´viations moyennes en bissection de lignes par patient pour chaque condition de stimulation. Base : ligne de base avant intervention ; preRC : avant la SGV cathode a` droite et anode a` gauche ; RC : pendant RC ; postRC : imme´diatement apre`s RC, postRC10 : 10 min apre`s RC ; presham : avant la stimulation simule´e ; sham : pendant la stimulation simule´e ; postsham : imme´diatement apre`s sham ; postsham10 : 10 min apre`s sham ; preLC : avant la SGV cathode a` gauche anode a` droite ; LC : pendant LC ; postLC : imme´diatement apre`s LC ; postLC10 : 10 min apre`s LC. 60 50 nombre d'étoiles barrées
tire´es de la batterie d’e´valuation de la ne´gligence (BEN) [30]. Chaque ligne e´tait pre´sente´e sur une feuille A4 dispose´e horizontalement en face du patient. Le patient devait marquer le centre de la ligne d’un trait de crayon. La de´viation en millime`tre par rapport au centre de la ligne e´tait mesure´e. Par convention les de´viations vers la droite e´taient note´es positivement, celles vers la gauche ne´gativement. La ligne de base a e´te´ mesure´e sur 8 bissections en moyenne (min 5, max 9) et en moyenne 4 bissections (min 3, max 5) ont e´te´ re´alise´es a` chaque temps de mesure avant, durant et apre`s les SGV. Les patients ont e´galement passe´ l’e´preuve de barrage d’e´toiles de la batterie « Behavioral Inattention Test » [31]. Le crite`re e´value´ e´tait le nombre total de petites e´toiles barre´es. Dans ce test, trois omissions signent un trouble attentionnel. Ce test n’e´tait passe´ qu’une fois avant, durant et apre`s les SGV. L’ordre d’administration des diffe´rentes stimulations est indique´ dans le Tableau 1. L’appareil utilise´ pour la SGV e´tait un ge´ne´rateur de courant continu re´gule´ (Galvadyn, Electronic Conseil, Gallargues Le Montueux, France ; courant de sortie : 20 mA max ; tension de sortie : 30 V max). Les e´lectrodes de carbone (4 cm 6 cm) e´taient recouvertes d’une e´ponge imbibe´e de se´rum physiologique et maintenues en place sur les mastoı¨des par un bandeau. Chaque patient a rec¸u 3 conditions de stimulation : cathode a` gauche–anode a` droite, la condition inverse et une stimulation simule´e. L’e´cart entre les stimulations e´tait d’au minimum 48 h pour e´viter que les re´sultats ne soient perturbe´s par un post-effet de la stimulation pre´ce´dente. Les patients n’e´taient pas informe´s du type de stimulation rec¸u au cours de chaque se´ance. Au cours des stimulations, l’intensite´ e´tait augmente´e manuellement de 0,1 mA par seconde jusqu’a` 1,5 mA. Lors de l’augmentation et de la diminution d’intensite´, la SGV peut entraıˆner une le´ge`re de´mangeaison. Pour cette raison, lors de la stimulation simule´e le courant e´tait augmente´ de la meˆme manie`re puis arreˆte´ apre`s quelques secondes. Les stimulations simule´es ont e´te´ effectue´es cathode sur la mastoı¨de gauche et anode sur la droite. De cette manie`re la distinction entre les stimulations re´elles et simule´es est impossible [32]. La stimulation durait 20 min pour chaque condition. Cette dure´e a e´te´ choisie en accord avec les crite`res de se´curite´ propose´s pour la stimulation transcraˆnienne par courant direct [33]. Les tests e´taient re´alise´s apre`s 10 minutes de stimulation. Une alarme pre´re´gle´e sonnait la fin de la stimulation et le stimulateur s’e´teignait automatiquement. L’analyse statistique des donne´es a e´te´ re´alise´e a` l’aide du logiciel R version 2.14.1 [34]. Le test de Friedman a e´te´ utilise´ pour la comparaison des moyennes des de´viations mesure´es pour chaque type de stimulation. Le test de Friedman est non parame´trique et permet de comparer k e´chantillons appareille´s correspondant a` k conditions the´rapeutiques portants sur les meˆmes blocs, afin de mettre en e´vidence une diffe´rence entre les conditions. Pour l’e´preuve de barrage, le test de Friedman a e´galement e´te´ utilise´ pour comparer le nombre total d’e´toiles barre´es. Tous les patients ont donne´ leur accord pour participer a` l’e´tude apre`s avoir e´te´ informe´ de son de´roulement, de ses objectifs et des risques lie´s a` la SGV, en accord avec la de´claration d’Helsinki.
575
40 Paent BP 30 20 10
Paent CB Paent FG Paent KJ moyenne
0
Fig. 2. Nombre d’e´toiles barre´es par patient pour chaque condition sur l’e´preuve de barrage d’e´toile du Behavioural Inattention Test. Base : ligne de base avant intervention ; preRC : avant la SGV cathode a` droite et anode a` gauche ; RC : pendant RC ; postRC : imme´diatement apre`s RC, postRC10 : 10 min apre`s RC ; presham : avant la stimulation simule´e ; sham : pendant la stimulation simule´e ; postsham : imme´diatement apre`s sham ; postsham10 : 10 min apre`s sham ; preLC : avant la SGV cathode a` gauche anode a` droite ; LC : pendant LC ; postLC : imme´diatement apre`s LC ; postLC10 : 10 min apre`s LC.
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Les patients FG et BP ont obtenu de meilleurs re´sultats aux deux tests lors de la stimulation cathode a` droite comme nous l’avions attendu. Les patients ont e´te´ syste´matiquement interroge´s sur les sensations ressenties lors des stimulations a` la fin de chaque se´ance. Le patient KJ a rapporte´ des sensations de bruˆlures sous l’e´lectrode mastoı¨dienne droite quel que soit le mode de stimulation mais sans que cela n’atteigne le seuil douloureux. La stimulation factice produisait e´galement cette sensation mais de fac¸on moins intense. Le patient avait une cicatrice de craniectomie de´compressive au-dessus de la mastoı¨de droite et des dysesthe´sies dans la re´gion re´tro-auriculaire. Les autres patients n’ont pas ressenti de douleur mais parfois une sensation de de´mangeaison sous l’e´lectrode. Aucune le´sion cutane´e n’a e´te´ observe´e sous les e´lectrodes. 2.4. Discussion La stimulation galvanique vestibulaire de modifiait pas significativement les re´sultats aux tests de bissection de ligne de 20 cm de la BEN et de barrage d’e´toiles du Behavioral Inattention Test (BIT). Les re´sultats ne confirment pas les travaux ante´rieurs [19,20]. Dans l’e´tude de Utz et al. [20], une variante du test de bissection de Schenkenberg e´tait propose´e comprenant 17 lignes a` barrer sur une feuille. Seules les bissections des lignes situe´es les plus a` droite sur la feuille e´taient significativement moins de´vie´es a` droite sous SGV. Le test de Schenkenberg est possiblement plus sensible aux variations de la NSU. Ne´anmoins, nos re´sultats ont montre´ que la SGV n’avait pas d’effet sur la de´viation en bissection d’une ligne unique place´e face au patient souffrant de ne´gligence gauche. Pour l’e´preuve de barrage, la SGV ne modifiait pas significativement le nombre total d’e´toiles barre´es. Dans l’e´tude de Rorsman et al. [19], la SGV avait permis d’augmenter le nombre de cibles barre´es sur les e´preuves de barrage de lignes et d’e´toiles du BIT. Ne´anmoins, cette ame´lioration e´tait inconstante et l’effet positif de la SGV n’e´tait pas affirmable sur les 2 tests en meˆme temps malgre´ un plus grand nombre de patients. Dans l’e´tude de Rorsman et al. une stimulation infraliminale ´etait propose´e avec une intensite´ de 0,7 a` 1,7 mA (me´diane : 1,15) uniquement pendant la re´alisation des tests [19]. Dans notre e´tude la me´thode de stimulation e´tait identique a` celle de Utz et al. [20] et n’explique donc pas la diffe´rence des re´sultats. En l’absence d’effet significatif, il est impossible de conclure sur la dure´e de cet effet. En revanche, comme de´crit dans la litte´rature, la SGV est simple en pratique, peu couˆteuse, bien tole´re´e. Aucun patient ne s’est plaint de douleurs et les sensations de de´mangeaisons sous l’e´lectrode sont un effet secondaire fre´quemment de´crit dans la litte´rature. Si la SGV est une technique peu contraignante, la question de son efficacite´ reste discutable nos re´sultats e´tant contradictoire avec ceux pre´ce´demment de´crit. Des intensite´s plus e´leve´es pourraient avoir des effets supe´rieurs mais risquent de rendre impossible la comparaison a` un placebo. Un autre moyen d’ame´liorer l’efficacite´ pourrait eˆtre d’augmenter le nombre de se´ances de stimulation. Cependant une e´tude re´cente a montre´ que l’ame´lioration des performances sur les tests du
BIT n’est pas plus importante apre`s 10 se´ances de SGV qu’apre`s une se´ance unique [35]. En l’absence de condition placebo, cette dernie`re e´tude portant sur un effectif large ne permet pas de conclure sur l’effet de la SGV. S’il existe, le me´canisme d’action de la SGV sur les symptoˆmes de NSU est mal e´lucide´. Le cortex parie´tal poste´rieur droit est active´ dans les taˆches de bissection et sa le´sion entraıˆne fre´quemment une NSU [36–38]. Lors d’une taˆche de bissection chez le sujet sain, la SGV entraıˆne une augmentation d’activation des cortex pre´moteur ventral et parie´tal poste´rieur droits en IRMf. L’activation corticale en IRMf est maximale sous SGV lors de la mise en marche et de l’arreˆt du courant continu [39,40]. L’effet sur la NSU d’une stimulation vestibulaire par courant alternatif serait inte´ressant a` e´tudier. Il semble que la stimulation cathode a` droite entraıˆne de meilleurs effets sur des taˆches d’exploration visuelle [19,20]. La configuration inverse paraıˆt plus efficace sur l’extinction sensitive [21]. Les modes de stimulation pourraient avoir des effets diffe´rents selon les patients et leur type de le´sions. La limite principale de cette e´tude est son faible effectif. De plus, seuls les patients e´taient aveugles au type de stimulation rec¸u. L’utilisation du test de bissection de Schenkenberg aurait permis une meilleure comparaison aux re´sultats de´ja` publie´s. Pour respecter les re`gles de se´curite´, l’exposition a` la SGV n’a pas exce´de´ 20 minutes ce qui limitait le nombre de test propose´ et le nombre d’essais par test. De nouvelles e´tudes sont ne´cessaires pour mieux comprendre le me´canisme d’action de la SGV et trouver des modalite´s de stimulation efficaces. 2.5. Conclusion La SGV ne diminuait pas la NSU sur des taˆches de bissection de ligne et de barrage en comparaison a` une condition simule´e dans notre e´tude. Des e´tudes supple´mentaires sont ne´cessaires pour comprendre les divergences avec les re´sultats de´ja` de´crits. Les effets de se´ances de re´pe´te´es, d’une SGV de plus forte intensite´ ou d’un courant alternatif me´riteraient d’eˆtre e´tudie´s pour ame´liorer cette technique avant d’envisager son utilisation en re´e´ducation. De´claration d’inte´reˆts Les auteurs n’ont pas transmis de de´claration de conflits d’inte´reˆts. References [1] Heilman KM, Valenstein E, Watson RT. Neglect and related disorders. Semin Neurol 2000;20:463–70. [2] Appelros P, Karlsson GM, Seiger A, Nydevik I. Neglect and anosognosia after first-ever stroke: incidence and relationship to disability. J Rehabil Med Off J UEMS Eur Board Phys Rehabil Med 2002;34:215–20. [3] Denes G, Semenza C, Stoppa E, Lis A. Unilateral spatial neglect and recovery from hemiplegia: a follow-up study. Brain 1982;105(Pt 3):543–52. [4] Jehkonen M, Ahonen JP, Dastidar P, Koivisto AM, Laippala P, Vilkki J, et al. Visual neglect as a predictor of functional outcome one year after stroke. Acta Neurol Scand 2000;101:195–201. [5] Paolucci S. The role of unilateral spatial neglect in rehabilitation of right brain[ndash]damaged ischemic stroke patients: a matched comparison. Arch Phys Med Rehabil 2001;82:743–9.
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