Drug-resistant temporal lobe epilepsy is associated with postural control abnormalities

Epilepsy & Behavior 21 (2011) 31–35

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Epilepsy & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / ye b e h

Drug-resistant temporal lobe epilepsy is associated with postural control abnormalities S. Colnat-Coulbois a,b,c,⁎, G.C. Gauchard a,b, L. Maillard d, J.P. Vignal d, H. Vespignani d, J. Auque c, Ph.P. Perrin a,b,e a

Balance Control and Motor Performance, UFR STAPS, Henri Poincaré University Nancy I, Villers-lès-Nancy, France Thematic Group “Neurodegenerative Diseases, Neuroplasticity, Cognition,” Faculty of Medicine, INSERM U 954, Vandoeuvre-lès-Nancy, France Department of Neurosurgery, University Hospital of Nancy, Nancy, France d Department of Neurology, University Hospital of Nancy, Nancy, France e Department of ENT, University Hospital of Nancy, Nancy, France b c

a r t i c l e

i n f o

Article history: Received 16 December 2010 Revised 11 February 2011 Accepted 19 February 2011 Available online 6 April 2011 Keywords: Temporal lobe epilepsy Balance control Antiepileptic drugs Posturography Vestibular function

a b s t r a c t Epilepsy is responsible for falls that are not systematically associated with seizures and that therefore suggest postural impairment. There are very few studies of postural control in patients with epilepsy and none of them focus on temporal lobe epilepsy (TLE), although part of the vestibular cortex is located in the temporal cortex. The aim of this study was to evaluate the characteristics of postural control in a homogeneous population of patients with complex partial TLE. Twenty-six patients with epilepsy and 26 age-matched healthy controls underwent a sensory organization test combining six conditions, with and without sensory conflicting situations. Patients with epilepsy displayed poorer postural control, especially in situations where vestibular information is necessary to control balance. In addition to potential antiepileptic drug side effects, vestibular dysfunction could be related to the temporal pathology. Our study allows for a better understanding of the mechanism underlying falls in this population of patients. © 2011 Elsevier Inc. All rights reserved.

1. Introduction Human postural control is a complex sensorimotor function requiring the central processing of neurosensorial afferents from the visual, somatokinesthetic, and vestibular systems to generate a context-specific motor response that leads to stabilization of antigravity activity and gaze and adjustment of static and dynamic postures according to the expected task and the cognitive and environmental contexts [1–3]. During normal standing (stable vision, fixed support), this information is redundant and complementary to a higher contribution of proprioceptive and visual inputs than to vestibular inputs to perceive postural sway [4]. The vestibular system, especially the otolithic organs, detects gravitational verticality, enabling the central nervous system to organize balance and posture according to the gravity reference frame and modulate postural tone [2,4,5]. However, if either the environmental or task conditions change, a switch between the sensory information is weighted according to the resulting balance difficulties and the gain of the different afferent postural loops is modified [5–7]. Damage to any of

⁎ Corresponding author at: Département de Neurochirurgie, CHU de Nancy, Hôpital Central, 29 Avenue de Lattre de Tassigny, 54000 Nancy, France. Fax: + 33 383 85 26 12. E-mail address: [email protected] (S. Colnat-Coulbois). 1525-5050/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2011.02.024

these balance regulation levels affects the output of the postural system, resulting in an increased risk of postural instability. Epilepsy is a disabling neurological disorder that is known to impair quality of life because of seizure frequency [8,9] and associated cognitive and affective disorders [8,10]. However, although falling is responsible for significant morbidity in patients with epilepsy [11], falls are not systematically associated with seizure [12], which suggests the involvement of subclinical balance impairments. Several posturographic studies have shown balance abnormalities in both children [13,14] and adults [15,16] with generalized or focal epilepsy. In all these studies, the groups with epilepsy were heterogeneous and the etiologies of the epilepsies varied. In addition, several studies have suggested that antiepileptic drugs (AEDs) may play a role in balance impairment [17–19], and it seems that it may be drug and dose related. Among patients with epilepsy, those with temporal lobe epilepsy (TLE) are of particular interest when considering the issue of balance dysfunction. Indeed, electrophysiological [20,21] and imaging [22–26] studies have demonstrated the involvement of temporal structures such as the temporal cortex and hippocampus in vestibular function. Nevertheless, to our knowledge, no study has ever investigated postural abnormalities associated with TLE. Our study was therefore designed with the aim of evaluating the characteristics of postural control in a homogeneous population of patients presenting with partial TLE.

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2. Materials and methods 2.1. Population The study involved 26 patients with intractable TLE (15 women, 11 men) (Table 1). They were recruited in the context of a presurgical evaluation of drug-resistant TLE. Mean duration of the disease was 13.6 ± 8 years. Temporal lobe epilepsy was diagnosed with ictal and interictal video/EEG recordings and imaging data (MRI, PET). Intracerebral recordings by stereo-electroencephalography (sEEG) were required in two cases. Epilepsy involved the right temporal lobe in 17 patients and the left temporal lobe in 9 patients. Twenty-three patients were right-handed and three were left-handed (handedness was evaluated according to the Edinburgh Inventory). All patients were treated with at least one AED, and 38% of patients were taking more than two AEDs. None of the patients had clinical signs of AED intoxication. Two patients spontaneously complained of vertigo. There was no history of falls or complaints of imbalance in this group. The control group (Table 1) comprised 26 age- and gendermatched self-declared healthy subjects. Exclusion criteria for patients and healthy subjects were: peripheral nervous system abnormalities, previous head or neck injuries, peripheral vestibular disease, and alcohol or drug addiction. In addition, healthy subjects were free of any pathology of the central nervous system and of any medication that might affect the central nervous system. All subjects gave their informed consent to participate in this study. 2.2. Posturography Posturographic recordings were carried out in a laboratory approved for biomedical research (Health Ministry agreement) using an EquiTest computerized dynamic posturography platform (Neurocom, Clackamas, OR, USA). The interval between the last seizure and the posturographic recording was greater than 48 hours in the patients. For each test, the subjects were requested to stand upright and barefoot, remaining as stable as possible and breathing normally with their arms at their sides, and were instructed to look straight ahead at a picture located on the visual surround at approximately 60 cm in the axis of the participant's glance. To protect against falls, all participants wore a safety harness connected to the ceiling by two suspension straps, in all test conditions. EquiTest uses a dual platform consisting of two footplates connected by a pin joint. The two footplates are supported by four force transducers (strain gauges) mounted symmetrically on a supporting center plate. Force data are sampled at 100 Hz and stored on a PC using a 12-bit A/D converter. A fifth transducer is bracketed to the center plate directly beneath the pin joint. The center transducer measures shear forces along the Y axis, in the plane parallel to the floor. The other transducers measure vertical forces applied to the dual platform. The data are filtered using a second-order Butterworth with 0 phase shift. The computer than calculates the center of pressure (CoP) and the vertical component of the center of gravity (CoG) using the subject height entered by the operator. The force transducers are placed so that when a subject stands with ankles

centered over the stripe on the dual platform, with feet equidistant laterally from the center line (Y axis), the CoG is located directly above the intersection of the X and Y axes (called electrical zero position, which serves as a reference point for the calculation of sway angles). The program uses small-angle approximation for arcsin x, which is accurate to 0.5% in the range of angles encountered. The Sensory Organization Test (SOT) consists of recording the CoP and interpreting the results obtained using various sensory inputs. To give inadequate information, somatosensory and visual cues are disrupted using a technique commonly referred to as swayreferenced, which involves tilting the support surface and/or the visual surround to directly follow the anterior–posterior sways of the subject's center of mass (CoM) (Fig. 1). The subject's task is to maintain an upright stance with as little postural sway as possible during the three 20-second trials in six conditions (Table 2). An equilibrium score is calculated by comparing the subject's anterior– posterior sway during each 20-second SOT trial with the maximal theoretical sway limits of stability. The theoretical limit of stability is based on the individual's height and the size of the support base. It represents an angle (8.5° anteriorly and 4.0° posteriorly) at which the person can lean in any direction before the center of gravity moves beyond a point that allows him or her to remain upright (i.e., the point of falling). The formula used to calculate the equilibrium score is [12.5° – ((θmax–θmin)/12.5°] × 100, where θmax is the greatest AP CoG sway angle displayed by the subject, and θmin is the lowest AP CoG sway angle. Lower sways lead to a higher composite score, indicating better balance control performance (a score of 100 represents no sway, whereas 0 indicates sway that exceeds the limit of stability, resulting in a fall). Equilibrium scores (ESs) are calculated for every condition: the average ESs of the three trials are C1ES in condition 1, C2ES in condition 2, C3ES in condition 3, C4ES in condition 4, C5ES in

Table 1 Characteristics of the population. Mean ± SD

Age (years) Height (m) Weight (kg) BMI (kg/m²) a

Group with epilepsy (n = 26)

Control group (n = 26)

33.7 ± 7.8 1.69 ± 0.10 70.5 ± 19.3 24.3 ± 4.8

35.2 ± 9.9 1.70 ± 0.08 67.3 ± 12.7 23.3 ± 2.8

NS, not significant.

Intergroup comparison

t = − 0.64, NSa t = − 0.07, NS t = 0.71, NS t = 0.96, NS

Fig. 1. EquiTest computerized dynamic posturography platform (Neurocom, Clackamas, OR, USA).

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Table 2 Sensory Organization Test: Determination of the six conditions and significance of sensory ratios. Conditions Name Condition Condition Condition Condition Condition Condition

1 (C1) 2 (C2) 3 (C3) 4 (C4) 5 (C5) 6 (C6)

Situation

Available cues

Unavailable or altered cues

Eyes open, fixed support Eyes closed, fixed support SRa surround, fixed support Eyes open, SR support Eyes closed, SR support SR surround, SR support

Vision, vestibular, somatosensory Vestibular, somatosensory Vestibular, somatosensory Vision, vestibular Vestibular Vestibular

— No vision Vision altered Somatosensory altered No vision, somatosensory altered Vision altered, somatosensory altered

Ratios Name Somatosensory (R VIS

Visual (R

SOM

)

)

Pair

Significance

C2/C1

Question: Does sway increase when visual cues are removed? Low scores: Poor use of somatosensory references. Question: Does sway increase when somatosensory cues are removed? Low scores: Poor use of visual references. Question: Does sway increase when visual cues are removed and somatosensory cues are inaccurate? Low scores: Poor use of vestibular cues or vestibular cues unavailable. Question: Do inaccurate visual cues result in increased sway compared with no visual cues? Low scores: Reliance on visual cues even inaccurate. Question: Do inaccurate somatosensory cues result in increased sway compared with accurate somatosensory cues? Low scores: Poor compensation for disruptions in selected sensory inputs.

C4/C1

Vestibular (RVEST)

C5/C1

Visual preference (RPREF)

(C3 + C6)/(C2 + C5)

Altered proprioceptive information management (RPMAN)

(C4 + C5 + C6)/(C1 + C2 + C3)

a

SR, sway-referenced.

condition 5, and C6ES in condition 6. Composite equilibrium scores (CES) are calculated to evaluate global balance performance by adding the average scores from conditions 1 and 2 and the ES from each trial of sensory conditions 3, 4, 5, and 6, and finally dividing that sum by the total number of trials, to smooth the data across all conditions. By using the individual scores for conditions 3, 4, 5, and 6, CES is effectively weighted to the more difficult conditions and characterizes the overall level of balance control performance, that is, coupling both simple and complex postural tasks (without and with sensory conflicts). Moreover, each ES is adjusted to C1ES to identify the significance of each sensory system influencing postural control, allowing determination of the use of somatosensory (RSOM), visual (RVIS), and vestibular (RVEST) information, as well as the ability to rely on vision even if inadequate (RPREF) and the ability to manage altered proprioceptive inputs (RPMAN) (see Table 2). In addition, SOT strategy scores are calculated to show the extent to which a patient uses ankle or hip movements to maintain equilibrium. A strategy score is derived from the fifth load cell in the platform, which is mounted in the center (under the X axis) and responds to horizontal shear forces. When CoG sway results only from the body rotating as a rigid mass around the ankle joints, there are no horizontal forces exerted along the Y axis against the support surface. In contrast, hip movements generate horizontal forces against the support surface that are proportional to the second derivative (angular acceleration) of the hip joint angle. During hip movement, the vertical force position changes only when the hip movement also causes changes in the CoG sway angle. Exclusive use of ankle strategy to maintain equilibrium results in a score of 100. Exclusive use of hip strategy yields a score close to 0. Strategy scores (SSs) between these two extremes represent a combination of the two strategies and are calculated for each condition (C1SS, C2SS, C3SS, C4SS, C5SS, C6SS). A composite strategy score (CSS) is calculated by independently averaging the scores for conditions 1 and 2, then adding the result to the equilibrium scores from each trial of sensory conditions 3, 4, 5, and 6, and finally dividing that sum by the total number of trials [27–31]. 2.3. Statistical analysis The statistics were produced with Statview Software (Abacus, Berkeley, CA, USA) using Student's t test (t, pairwise comparison) to compare the two groups with respect to SOT parameters, as well as

age, height, weight, and body mass index as described earlier. Statistically significant differences were accepted for a probability level of P ≤ 0.05, and borderline significance was defined as a probability level of P ≤ 0.10. 3. Results Data on age, height, weight, and body mass index for both groups are summarized in Table 1. No significant between-group differences were observed for any of the parameters. In the SOT (Table 3), postural performance was poorer in the patients with epilepsy than in the control group. In terms of equilibrium, statistically significant differences explained by lower performance in conditions 3, 5, and 6 were observed for the global score (CES). In addition, sensory analysis revealed lower RVEST and RPMAN values in the group with epilepsy than in the control group. Consequently, in terms of strategy scores, global performance was found to be lower in the epilepsy group (CSS), with statistically significant differences being observed in conditions 5 and 6 and differences of borderline significance in condition 4. 4. Discussion This study, which evaluated postural control during quiet stance, with and without sensory conflict, showed that patients with TLE exhibit more postural instability than healthy controls. They displayed more difficulties in ensuring balance, especially in more complex postural situations in which either vestibular information was the only reliable cue or sensory conflict was important. Moreover, they also exhibited more difficulties using vestibular information to control balance and to manage disrupted somatosensory information. Patients with epilepsy thus used hip joint movement more than the other patients to control balance, suggesting a less appropriate balance strategy. Conventionally, balance during quiet stance is supported by the use of an inverted pendulum model [32], and its regulation and adaptation to the environment are based on postural tone and on postural reflexes generated by the vestibular, visual, and somatosensory systems involving higher levels of control [33]. When postural situations are more complex, that is, in quiet stance situations with sensory conflicts or in dynamic situations, good performance in these tests is conveyed by the use of an anticipatory

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Table 3 Sensory Organization Test (SOT): equilibrium (ES) and strategy (SS) scores for the six conditions, the composite equilibrium score, and the different ratios (RSOM, RVIS, RVEST, RPREF and RPMAN) observed for the two groups. Statistical significance: p ≤ 0.05; borderline significance: p ≤ 0.10; NS: not significant. SOT

Mean ± SD Group with epilepsy (n = 26)

Equilibrium C1ES C2ES C3ES C4ES C5ES C6ES CES Ratios RSOM RVIS RVEST RPREF RPMAN

scores 93.25 ± 4.79 89.53 ± 8.72 88.36 ± 8.73 79.21 ± 19.74 57.51 ± 23.58 63.20 ± 23.25 74.83 ± 16.10

94.68 ± 3.22 92.51 ± 4.67 92.55 ± 3.33 85.97 ± 7.93 70.72 ± 9.51 76.28 ± 6.61 83.12 ± 4.39

t = − 1.29, t = − 1.57, t = − 2.33, t = − 1.65, t = − 2.70, t = − 2.81, t = − 2.58,

NSa NS P = 0.024 NS P = 0.009 P = 0.007 P = 0.013

0.96 ± 0.06 0.84 ± 0.20 0.61 ± 0.25 1.03 ± 0.10 0.72 ± 0.22

0.98 ± 0.03 0.91 ± 0.07 0.75 ± 0.11 1.04 ± 0.05 0.83 ± 0.06

t = − 1.38, t = − 1.60, t = − 2.72, t = − 0.11, t = − 2.55,

NS NS P = 0.009 NS P = 0.014

93.95 ± 2.32 93.51 ± 2.27 92.82 ± 3.13 85.92 ± 5.06 78.87 ± 3.71 80.69 ± 4.14 85.88 ± 2.92

t = − 1.41, t = − 1.52, t = − 1.61, t = − 1.90, t = − 2.96, t = − 2.93, t = − 2.68,

NS NS NS P = 0.063 P = 0.005 P = 0.005 P = 0.010

Strategy scores 92.01 ± 6.71 C1SS C2SS 91.42 ± 6.78 SS C3 90.53 ± 6.71 SS C4 79.47 ± 16.93 SS C5 68.40 ± 18.00 SS C6 68.41 ± 21.36 CSS 78.85 ± 13.32 a

Control group (n = 26)

Intergroup comparison

NS, not significant.

strategy, involving the ankle joint rather than the hip joint [34]. In our study, patients with epilepsy exhibited balance disorders particularly in complex situations. These results are consistent with those obtained by Petty et al., who showed that chronic antiepileptic treatment users had balance disorders especially in anterior–posterior and medial–lateral tilting platform situations [16]. Thus, it seems that although balance in quiet stance is relatively preserved in patients with TLE, more complex situations reveal balance impairment suggestive of central integration processing disruption. Our posturographic results show that central vestibular functions could be impaired, which is consistent with the known relationship between vestibular function and the temporal lobe. Many studies have contributed to the localization of part of the human vestibular cortex in the temporal lobe. Penfield induced vestibular responses in a patient by stimulating the cortex of the gyrus of Heschl [20]. Kahane et al. [21] proposed a mapping of the human vestibular cortex in a population of patients with epilepsy undergoing intracerebral recordings: they obtained vestibular responses after electrical stimulation of the posterior part of the superior temporal gyrus and the temporoparietal cortex. Fasold et al. [25], using functional MRI, identified cortical activation in the temporoparietal junction after caloric stimulation. Suzuki et al. [24] similarly reported activation of the superior temporal gyrus and hippocampus after caloric stimulation. Vestibular cortical function is located predominantly in the right hemisphere [25] or, more precisely, in the nondominant hemisphere [35]. It is well known that TLE is associated with impairment of some temporal functions such as verbal, nonverbal, and visuospatial memory [36,37]. Thus, it is possible that temporal vestibular function is impaired in refractory TLE. The effects of AEDs, however, also need to be considered in relation to postural control and epilepsy. In our study, 38% of the patients with epilepsy were treated with a combination of AEDs. Most AEDs induce adverse effects such as imbalance and ataxia [17], although those symptoms seem to be more frequently observed with carbamazepine. Fife et al. [19] assessed the effects of three different AEDs on balance in

older people and reported that patients on lamotrigine displayed better dynamic performance than patients on carbamazepine. Remi et al. [18] observed postural abnormalities in healthy subjects after pregabalin and carbamazepine intake. Petty et al. [16] reported balance impairment in chronic AED users compared with healthy subjects. However, the mechanism of drug-related balance impairment remains unclear and appears to be influenced by several factors such as cerebellar and vestibular dysfunction [17]. Some features may be specifically implicated. Indeed, our hypothesis is that postural abnormalities can be explained in our patients by a combination of temporal vestibular dysfunction related to chronic epilepsy and drug side effects. However, it is difficult to differentiate the respective roles of the two factors as it is not possible to assess a control population of patients with refractory TLE not taking AEDs. Although this was not the aim of the present study, choosing a different control group, comprising patients with extratemporal epilepsy or patients taking AEDs for nonepilepsy reasons, could have assessed the influence of AEDs. It could constitute a new field of investigation in future studies. In addition, our study does not allow us to distinguish whether the results observed reflect exclusive impairment of the central or peripheral vestibular functions, even if the central hypothesis seems a more valid theory considering the pathology. 5. Conclusion This study showed balance abnormalities in patients with temporal lobe epilepsy, especially in situations where central vestibular information processing is essential for organizing balance control. Although this study addresses the issue of imbalance in patients with epilepsy in a very technical manner, these results may be used to better anticipate fall-related morbidity in this patient population who also have to cope with sensory conflicting situations on a daily basis. References [1] Fransson P, Johansson R, Hafstrom A, Magnusson M. Methods for evaluation of postural control adaptation. Gait Posture 2000;12:14–24. [2] Keshner EA, Allum JH, Pfaltz CR. Postural coactivation and adaptation in the sway stabilizing responses of normals and patients with bilateral vestibular deficit. Exp Brain Res 1987;69:77–92. [3] Massion J. Postural control system. Curr Opin Neurobiol 1994;4:877–87. [4] Fitzpatrick R, McCloskey DI. Proprioceptive, visual and vestibular thresholds for the perception of sway during standing in humans. J Physiol 1994;478:173–86. [5] Peterka RJ. Sensorimotor integration in human postural control. J Neurophysiol 2002;88:1097–118. [6] Bronstein AM, Hood JD, Gresty MA, Panagi C. Visual control of balance in cerebellar and parkinsonian syndromes. Brain 1990;113(Pt, 3):767–79. [7] Marsden CD, Merton PA, Morton HB. Human postural responses. Brain 1981;104: 513–34. [8] Park SP, Song HS, Hwang YH, Lee HW, Suh CK, Kwon SH. Differential effects of seizure control and affective symptoms on quality of life in people with epilepsy. Epilepsy Behav 2010;18:455–9. [9] Djibuti M, Shakarishvili R. Influence of clinical, demographic, and socioeconomic variables on quality of life in patients with epilepsy: findings from Georgian study. J Neurol Neurosurg Psychiatry 2003;74:570–3. [10] Tracy JI, Dechant V, Sperling MR, Cho R, Glosser D. The association of mood with quality of life ratings in epilepsy. Neurology 2007;68:1101–7. [11] Wirrel H. Epilepsy related injuries. Epilepsia 2006;47(Suppl 1):79–86. [12] Ensrud KE, Blackwell TL, Mangione CM, et al. Central nervous system-active medications and risk for falls in older women. J Am Geriatr Soc 2002;50:1629–37. [13] Beckung E, Uvebrant P. Impairments, disabilities and handicaps in children and adolescents with epilepsy. Acta Paediatr 1997;86:254–60. [14] Van Mil SG, de la Parra NM, Reijs RP, van Hall MH, Aldenkamp AP. Psychomotor and motor functioning in children with cryptogenic localization related epilepsy. NeuroRehabilitation 2010;26:291–7. [15] Gandelman-Marton R, Arlazoroff A, Dvir Z. Balance performance in adult epilepsy patients. Seizure 2006;15:582–9. [16] Petty SJ, Hill KD, Haber NE, et al. Balance impairment in chronic antiepileptic drug users: a twin and sibling study. Epilepsia 2010;51:280–8. [17] Sirven JI, Fife TD, Wingerchuk DM, Drazkowski JF. Second-generation antiepileptic drugs' impact on balance: a meta-analysis. Mayo Clin Proc 2007;82:40–7. [18] Remi J, Huttenbrenner A, Feddersen B, Noachtar S. Carbamazepine but not pregabalin impairs eye control: a study on acute objective CNS side effects in healthy volunteers. Epilepsy Res 2010;88:145–50.

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