Epilepsy & Behavior 22 (2011) 718722

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Epilepsy & Behavior

journal homepage: www.elsevier.com/locate/yebeh

Physiological and electroencephalographic responses to acute exhaustive physical

exercise in people with juvenile myoclonic epilepsy
Cristiano de Lima a, Rodrigo Luiz Vancini b, Ricardo Mario Arida b, Laura M.F.F. Guilhoto c,
Marco Tlio de Mello a, Amaury Tavares Barreto a, Mirian Salvadori Bittar Guaranha c,
Elza Mrcia Targas Yacubian c, Sergio Tuk a,
a
Departamento de Psicobiologia, Universidade Federal de So Paulo, So Paulo (SP), Brazil
b
Departamento de Fisiologia, Universidade Federal de So Paulo, So Paulo (SP), Brazil
c
Departamento de Neurologia, Unidade de Pesquisa e Tratamento das Epilepsias da Universidade Federal de So Paulo, So Paulo (SP), Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Although the available evidence suggests that exercise may positively affect epilepsy, whether this effect is
Received 20 June 2011 applicable to different types of epilepsy has not been established. Physiological responses during rest,
Revised 2 August 2011 acute physical effort, and a recovery period were studied by concomitant analysis of cerebral electric activity
Accepted 26 August 2011
using EEGs in subjects with juvenile myoclonic epilepsy (JME) and healthy controls. In addition, level of
Available online 4 October 2011
habitual physical activity, body composition, and 1 week of actigraphy monitoring data were evaluated.
Keywords:
Twenty-four subjects (12 with JME and 12 controls) participated in this study. Compared with the control
Epilepsy group, the JME group had a signicantly lower VO2 at rest (13.3%) and resting metabolic rate (15.6%). The
Seizure number of epileptiform discharges in the JME group was signicantly reduced during the recovery period
Sleep (72%) compared with the resting state. There were no signicant differences between the JME and control
Physical activity groups in behavioral outcomes and sleep parameters evaluated by actigraphy monitoring. The positive
Resting metabolic rate ndings of our study strengthen the evidence for the benets of physical exercise for people with JME.
Electroencephalogram 2011 Published by Elsevier Inc.

1. Introduction promoted positive plastic changes in the hippocampal formation such

In the last ve decades, there has been much research on the rela-
tionship between epilepsy and physical exercise. Positive effects
of exercise on seizure frequency and severity [1,2] have been demon-
strated, suggesting that exercise may have a protective effect on
people with epilepsy [3,4]. Information concerning the acute [5,6] and
chronic [1,2,7,8] physiological responses to exercise in individuals
with epilepsy have revealed poor cardiorespiratory tness [6,9,10]
and lower levels of strength [7,8] and exibility [7]. In contrast, it has
been shown that physical exercise can induce positive effects such as
a decrease in epileptiform discharges during physical effort and the re-
covery period, compared with the resting state [3,6,11], as well as di-
minished predisposition to and better control of seizures [1,3,1214].
From an experimental point of view, these effects have also been
observed in animal models of temporal lobe epilepsy [1520]. For in-
stance, in rats with epilepsy, physical exercise retarded the develop-
ment of amygdala kindling [15], reduced seizure frequency [16], and
Corresponding author at: Universidade Federal de So Paulo (UNIFESP), Rua
Botucatu, 862, 1 andar, 04023062 So Paulo, SP, Brazil. Fax: + 55 11 5572 5092.
E-mail address: stuk@psicobio.epm.br (S. Tuk).
as decreased CA1 hyperresponsiveness [18] and prominent changes in
the staining of parvalbumin, a calcium-binding protein, in the dentate
gyrus [19].
Despite the encouraging ndings reported above, the existing
clinical data on the impact of exercise on epilepsy have limitations.
The majority of subjects analyzed had different types of epilepsy,
controlled or refractory epilepsy, and were either physically active
or inactive. Therefore, we have to take into account whether the bene-
cial effects of exercise are also applicable to a particular type of epilep-
sy. In this context, we selected subjects with juvenile myoclonic
epilepsy (JME), a type of epilepsy that constitutes 511% of all epilepsy
cases [21,22] and often arises in the second decade of life. JME is charac-
terized by myoclonic onset on awakening, tonicclonic seizures, and,
less frequently, absence seizures [23]. Because people with epilepsy
are often overprotected and typically lead sedentary lifestyles, this
group also tends to be physically unt [24]. Considering that people
with epilepsy can participate in regular physical exercise programs
and also in daily activities that comprise physical efforts consisting of
aerobic and anaerobic components, we investigated whether intensive
exercise alters seizure susceptibility in JME.
In this context, we evaluated physiological variables during acute
physical effort with concomitant analysis of cerebral electric activity

1525-5050/$ see front matter 2011 Published by Elsevier Inc.

doi:10.1016/j.yebeh.2011.08.033
 C. de Lima et al. / Epilepsy & Behavior 22 (2011) 718722
using EEGs. In addition, sleep/wake cycle, level of habitual physical
activity, body composition, resting metabolic rate, and aerobic tness
were evaluated.
2. Methods
2.1. Subjects
People with JME were recruited from an epilepsy treatment unit at
the Federal University of So Paulo. They were initially contacted in
the unit during their routine medical care and informed about the
purpose of the study. Of the 12 contacts made, all individuals with
JME agreed to participate in the study. The control group consisted
of healthy subjects recruited among students and staff from the
Federal University of So Paulo and was matched with respect to
gender, age, and level of physical activity. Therefore, this cross-
sectional and controlled study involved a total of 24 individuals
from 16 to 45 years of age split into the control (32.1 6.5 years,
n = 12) and JME (26.4 7.6 years, n = 12) groups.
Both groups underwent the following phases of testing: a medical
record and physical examination, an ECG at rest and during effort,
evaluation of anthropometry and body composition, 1 week of
actigraphy monitoring, evaluation of resting metabolic rate, and
an incremental exercise test (acute physical effort) concomitantly
with an EEG exam. A questionnaire on habitual physical activity was
distributed to the volunteers to be answered in a quiet room before
the physical test.
Exclusion criteria included any progressive neurological disorder
(with the exception of epilepsy among the JME group), cognitive
impairment, and history of cardiovascular, pulmonary, orthopedic, or
endocrinological disease. Subjects with JME were included if they had
had JME for at least 3 years, had been diagnosed with JME according
to the 1989 International League Against Epilepsy criteria, experienced
controlled tonicclonic seizures, and were compliant with medication
[25]. This study was approved by the Federal University of Sao Paulo's
Research Ethics Committee, and all participants signed informed
consent forms prior to participating. Parents signed the informed
consent form for those subjects younger than 18 years of age.
2.2. Behavioral measures: Habitual physical activity questionnaire
Habitual level of physical activity of the control and JME groups
was evaluated with the Baecke questionnaire. This questionnaire con-
sists of 16 questions involving three habitual physical activity scores
relating to the preceding 12 months: Occupational Physical Activity
(8 questions), Physical Exercise during Leisure Time (4 questions),
and Leisure and Locomotion Activities (4 questions). The total
score for habitual physical activity was obtained by summing the
Occupational Physical Activity, Physical Exercise during Leisure,
and Leisure and Locomotion Activity scores: the higher the score,
the higher the level of habitual physical activity [26].
2.2.1. Body composition
Subjects from the control and JME groups wearing light clothing and
no shoes were weighed on a Filizola scale to the nearest 0.1 kg. Height
was measured to the nearest 0.5 cm by means of a wall-mounted stadi-
ometer (Sanny, Model ES 2030). Body composition, fat-free mass (kg)
and fat mass (kg), was estimated by plethismography using the BOD
POD system (Version 1.69, Life Measurement Instruments, Concord,
CA, USA) [27].
2.3. Actigraphy
Actigraphy is based on the principle that there is reduced move-
ment during sleep and increased movement during wakefulness.
Subjects from both groups (control and JME) used the actigraph (Mini
719
Motionlogger Actigraph/Octogonal Basic, Ambulatory Monitoring, Inc.,
Ardsley, NY, USA) continuously for 1 week before the acute physical
effort evaluation because of the vulnerability of subjects with JME
to generalized seizures when they are deprived of sleep. Data for the
control and JME groups were collected using the zero crossing mode
in 1-minute epochs. In addition, a sleep diary was given to each subject
during the same period. The sleep parameters analyzed were total sleep
time (TST), wake after sleep onset (WASO), and sleep percentage (%),
which was adopted as sleep efciency (SE) [28].
2.4. Physiological evaluation
The physiological variables of the control and JME groups were
veried rst during a resting state (for 30 minutes), then during acute
physical effort until volitional fatigue of the volunteer, and nally after
physical effort (for 30 minutes).
2.4.1. Resting metabolic rate
With the FitMate Metabolic System (Cosmed, Rome, Italy), resting
metabolic rate (RMR) was estimated for 15 minutes with the subjects
lying down. This system is capable of measuring oxygen consumption
and energy expenditure during rest and physical exercise [29]. Oxygen
consumption was collected and analyzed in 30-second intervals
with the subject in a face mask. An estimate of the energy expenditure
(kcal day- 1, representing 24 hours) was calculated with the same
equipment according to Weir [30]. In addition, the RMR values obtained
were compared with the predicted values and calculated and classied
according to Harris and Benedict [31].
2.4.2. Incremental exercise test
A graded maximal exercise test was administrated to the control
and JME groups to determine VO2max. The subjects were given a stan-
dardized set of instructions explaining the tests. After these prelimi-
nary procedures, each subject was submitted to an incremental
maximal exercise test on a mechanical cycle ergometer (Monark
Ergomedic 824E). The test schedule consisted of a 5-minute warmup
followed by progressive load increases at the rate of 12 W every
1 minute until volitional subject exhaustion according to the subject's
cardiorespiratory tness. During the exercise test, subjects were
verbally encouraged to exercise for as long as possible. VO2max
was evaluated with the FitMate Metabolic System [29]. Heart
rate (HR) during the test was recorded using a HR monitor (Polar
Electronics, Finland).
2.4.3. Electroencephalography registration
Video/EEG (Ceegraph software, Biologic Systems Corp.) monitor-
ing using 1020 international electrode placement with Collodion
was performed during the resting state with subjects lying down
(25 minutes) and seated (5 minutes) and both during the incremen-
tal exercise test (until volitional fatigue of the subject) and on recov-
ery after physical effort, with subjects seated (5 minutes) and lying
down (25 minutes). An EEG board-certied neurologist (L.M.F.F.G.)
counted the number of epileptiform discharges during the rest and
recovery periods. This procedure was carried out for both the control
and JME groups to establish the electroencephalographic prole of
each individual. The volunteers were linked to the metabolic system
for monitoring of physiological parameters during all phases of the
experiment.
2.5. Statistical analyses
Data are expressed as means SD. Normal distribution and homo-
geneity of the variances were determined using the Kolmogorov
Smirnov test. The difference between two measures was established
with Student's t test for unpaired and paired samples. Statistical
720 C. de Lima et al. / Epilepsy & Behavior 22 (2011) 718722

Table 1 Table 3
Body composition and anthropometric prole of the control and juvenile myoclonic Occupational Physical Activity, Physical Activity in Leisure, Sport Physical Activity,
epilepsy groups. and Total scores on the Baecke Questionnaire in the juvenile myoclonic epilepsy and
control groups.
Variable Control group JME group
(n = 12) (n = 12) Control group JME group P value
(n = 12) (n = 12)
Age (years) 32.1 6.5 26.4 7.6
Height (cm) 174.3 4.4 178.4 8.1 Occupational Physical Activity 2.38 0.19 2.05 0.35 0.4343
Body mass (kg) 80.7 17.3 74.2 16.3 Physical Activity in Leisure 2.85 0.18 3.20 0.14 0.1710
Free fat mass (kg) 63.0 9.4 61.4 9.1 Sport Physical Activity 2.56 0.16 2.60 0.18 0.8695
Fat mass (kg) 17.8 12.6 12.8 8.3 Total 7.80 0.33 7.84 0.41 0.9253

Note. Data are expressed as means SD. Note. Data are expressed as means SD.

analyses were conducted using Graph Pad Prism software (San
Diego, CA, USA).
3. Results
3.1. Subjects
Body composition and the anthropometric prole of the JME and
control groups are summarized in Table 1. No signicant differences
with respect to mean age (years), height (cm), body mass (kg), fat-
free mass (kg), or fat mass (kg) were observed between the two groups.
Duration of epilepsy, seizure frequency, seizure type, and antiepileptic
drugs (AEDs) for the JME group are listed in Table 2.
249.1) than in the contol group (1989.0 185.0). There were no sig-
nicant differences in the other variables measured at rest: FeO2 (%),
ventilation (L min- 1), respiratory rate (breaths min- 1). In the incre-
mental exercise test, there were no signicant differences in the vari-
ables analyzed: VO2max (mL kg- 1 min- 1), maximal load (watts), and
HRmax (beats min- 1) (Table 5). None of the subjects with JME had sei-
zures during the resting state, acute physical effort, or the recovery
period. A signicant reduction of 72% (t = 3.374, P = 0.0062, effect
size= 0.71) in the mean number of epileptic discharges (3- to 4-Hz
spikewave complexes) was observed in the recovery period
(1.4 1.8, n = 12) compared with the resting state (5.0 4.2, n = 12).
4. Discussion

3.2. Behavioral measures This study demonstrates that when submitted to progressive
exercise to exhaustion, subjects with JME had a reduced number
There were no signicant differences between the control and of epileptic discharges in the recovery period compared with the resting
JME groups in Occupational Physical Activity, Physical Activity during state. These ndings support previous observations that, in general,
Leisure Time, Sport Physical Activity, or Total score (Table 3). physical exercise is not a seizure-inducing factor [1,3,1214].
The level of habitual physical activity evaluated with the Baecke
3.3. Actigraphy questionnaire did not differ between the JME and control groups, as
demonstrated in other studies [9,32,33]. Most research on this topic
The mean values of TST, WASO and SE obtained by actigraphy has employed samples of individuals with different types of epilepsy;
monitoring in summarized in Table 4. These sleep parameters did in this regard, it cannot truly provide us with information about
not signicantly differ between the JME and control groups. this subject. For example, a recent study conducted by our research
group that analyzed only individuals with temporal lobe epilepsy
3.4. Physiological evaluation (TLE), the most common form of partial epilepsy, also reported
lower levels of leisure physical activity in patients with epilepsy
Among the physiological variables measured at rest, VO2 (mL min- 1) as compared with healthy subjects [6]. The inconsistent ndings
was signicantly lower (13.3%, t = 2.849, P = 0.0093, effect size = 0.52) could be attributed to the type of epilepsy, that is, JME. Accordingly,
in the JME group (244.4 32.0) than in the control group (282.2 Azevedo and collaborators [34] recently reported that people with
32.8). Consequently, RMR (kcal day- 1) was signicantly lower (15.6%, JME have better quality of life and, consequently, better health status
t = 3.474, p = 0.0022, effect size = 0.60) in the JME group (1678.0 when compared with individuals with TLE.
Studies of associations between the sleep/wake cycle and epilepsy
have demonstrated that AEDs and seizures can alter sleep patterns.
It has also been demonstrated that seizures in JME are dependent
Table 2
on the sleep/wake cycle and precipitant factors, sleep deprivation
Characteristics of the juvenile myoclonic epilepsy group.
being one of the most important factors. Sleep deprivation is the
Patient Age Duration of Seizure Seizure AEDs best method for provoking EEG epileptiform abnormalities [3537]
(years) epilepsy frequency type and seizures [38] in most types of epilepsy. Some forms of generalized
(years)
epilepsy, such as JME, are particularly sensitive to sleep deprivation
1 31 16 Controlled GTCS/M/A VPAa with motor jerk phenomena [39,40]. In this context, we evaluated
2 33 26 Controlled GTCS/M/A VPA
3 41 25 Weekly GTCS/M/A VPA/TPM
4 25 18 Controlled GTCS/M/A LTG/TPM
5 24 11 Controlled GTCS/M/A TPM
6 18 5 Controlled GTCS/M/A VPA/CBZ Table 4
7 25 8 Controlled GTCS/M/A LTG Sleep parameters (1-week averages) estimated by actigraphy recordings.
8 16 3 Controlled GTCS/M/A VPA
Variable Control group JME group P value
9 22 9 Controlled GTCS/M/A TPM
(n = 12) (n = 12)
10 27 25 Controlled GTCS/M/A VPA
11 36 25 Controlled GTCS/M/A VPA Total sleep time (min) 390.7 24.7 408.0 18.1 0.5767
12 18 5 Controlled GTCS/M/A VPA Wake after sleep onset (min) 16.6 2.2 26.2 5.6 0.1271
a Sleep efciency (%) 90.0 2.7 88.9 2.8 0.7743
GTCS, generalized tonicclonic seizures; M, myoclonic seizures; A, absence seizures;
VPA, valproate; TPM, topiramate; LTG, lamotrigine; CBZ, carbmazepine. Note. Data are expressed as means SD.
 C. de Lima et al. / Epilepsy & Behavior 22 (2011) 718722
Table 5
Physiological variables obtained in the resting state and incremental exercise test in
the control and juvenile myoclonic epilepsy groups.
Variable Control group JME group
(n = 12) (n = 12)
Resting state
VO2 (mL min- 1) 282.2 32.8 244.4 32.0a
FeO2 (%) 16.4 1.1 16.2 0.6
Ventilation (L min- 1) 7.8 0.9 7.0 1.2
RR (breaths min- 1) 12.9 3.9 12.6 3.2
RMR (kcal day- 1) 1989.0 185.0 1678.0 249.1a
Incremental exercise test
VO2max (mL kg- 1 min- 1) 37.13 7.13 35.68 8.70
Maximal load (W) 251.0 42.6 221.0 37.4
HRmax (beats min- 1) 178.9 9.2 179.2 10.2
Note. Data are expressed as means SD. VO2, oxygen uptake, RMR, resting metabolic
rate; FeO2, expired fraction of O2; RR, respiratory rate; HR, heart rate; max, maximal.
a
Statistically signicant difference relative to the control group (Student's t test for
unpaired samples, P b 0.05).
the sleep/wake cycle using actigraphy methodology during the 7 days
preceding the acute physical effort. Although in the present study,
the data for the JME group and those for the control group did not
differ signicantly, greater WASO and reduced SE were observed
in the JME group compared with the control group.
The analysis of physiological parameters demonstrated a lower
RMR and resting VO2 in subjects with JME. We must bear in mind
that in both groups, the results for both age and body mass were con-
sidered normal [30,31,41]. This difference might be attributed to a
lower free fat mass (2.5%) and body mass (8.0%) in the JME group.
Moreover, most of the commonly used anticonvulsants can inuence
nutritional status. In particular, some drugs affect regulation of energy
balance, with consequent loss (topiramate) or gain (carbamazepine
and valproate) of body weight [4245]. Among the subjects with
JME in our study, 58.3% were taking valproate. To this point, Bergqvist
et al. [46] demonstrated that resting energy expenditure adjusted
for free fat mass was signicantly lower in children with intractable
epilepsy than in healthy controls.
The physiological variables evaluated during the incremental
exercise test did not signicantly differ between the JME and control
groups. People with epilepsy typically have lower physical tness
[6,12,32,47]. One of the main parameters evaluated during physical ef-
fort is VO2max, which is directly correlated with cardiorespiratory tness
[48]. There were no signicant differences in VO2max values between the
JME (35.68 mL kg- 1 min- 1) and control (37.13 mL kg- 1 min- 1) groups.
For both groups, the results of the present study are in accordance
with the norm provided by Neder et al. [49] for cycle ergometry in the
Brazilian population.
In the present work, the number of epileptiform discharges in the
JME group was reduced in the recovery period compared with the
resting state. Although we acknowledge some possible limitations in
counting the discharges, we used only periods with no movements,
that is, rest and recovery phases. The classic study of Gtze et al. [3]
demonstrated that one session of exhausting physical exercise was
able to reduce epileptiform discharges on the EEG and increase the
threshold for seizure manifestation. As reported in several studies,
physical exercise may not be considered a seizure-inducing factor
[2,6,16,50,51]. Our ndings are in agreement with the literature
because none of the subjects in the JME group had seizures before,
during, or after physical exertion. Nevertheless, these ndings need to
be interpreted with caution because the current study has methodolog-
ical limitations. The problems in performing studies with people with
epilepsy are related to the great heterogeneity of the sample, difculty
in subject recruitment, low motivation, and fear of having seizures
during physical effort. However, our data were obtained in a specic
epilepsy population.
721
In summary, our results demonstrate that people with JME and
healthy subjects have similar levels of physical activity, sleep pa-
rameters, and values of physiological variables. The main nding of
P value this study is that in individuals with JME, the number of discharges
on the EEG decreases after physical exercise. These ndings may
have clinical relevancy; knowing the benecial effects of exercise on
0.0093 general health, individuals with JME should be included in physical
0.6601
exercise programs that could lead to reduction in seizure occurrence
0.1181
0.8580 and improved quality of life.
0.0022
Acknowledgments
0.6589
0.0805 Research was supported by CNPq, FAPESP, CAPES, and AFIP.
0.9502 The authors thank all of the subjects who volunteered their time
to participate in this study.
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