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Arquivos de Neuro-Psiquiatria

Print version ISSN 0004-282X

Arq. Neuro-Psiquiatr. vol.73 no.1 São Paulo Jan. 2015

http://dx.doi.org/10.1590/0004-282X20140188 

Articles

Low levels of maximal aerobic power impair the profile of mood state in individuals with temporal lobe epilepsy

Os baixos níveis de potência aeróbia máxima prejudicam o perfil do estado de humor em indivíduos com epilepsia do lobo temporal

Rodrigo Luiz Vancini 1  

Claudio Andre Barbosa de Lira 2  

Marília dos Santos Andrade 3  

Cristiano de Lima 4  

Ricardo Mario Arida 3  

1Centro de Educação Física e Desportos, Universidade Federal do Espírito Santo, Vitória ES, Brazil;

2Setor de Fisiologia Humana e do Exercício, Faculdade de Educação Física e Dança, Universidade Federal de Goiás, Goiânia GO, Brazil;

3Departamento de Fisiologia, Universidade Federal de São Paulo, Sao Paulo SP, Brazil;

4Departamento de Psicobiologia, Universidade Federal de São Paulo, Sao Paulo SP, Brazil.

ABSTRACT

Objective

To investigate the correlation between cardiorespiratory fitness and mood state in individuals with temporal lobe epilepsy (TLE).

Method

Individuals with TLE (n = 20) and healthy control subjects (C, n = 20) were evaluated. Self-rating questionnaires were used to assess mood (POMS) and habitual physical activity (BAECKE). Cardiorespiratory fitness was evaluated by a maximal incremental test.

Results

People with TLE presented lower cardiorespiratory fitness; higher levels of mood disorders; and lower levels of vigor when compared to control health subjects. A significant negative correlation was observed between the levels of tension-anxiety and maximal aerobic power.

Conclusion

Low levels of cardiorespiratory fitness may modify the health status of individuals with TLE and it may be considered a risk factor for the development of mood disorders.

Key words: epilepsy; profile of mood state; POMS; physical activity; exercise; cardiorespiratory fitness

RESUMO

Objetivo

Investigar a correlação entre aptidão cardiorrespiratória e variáveis de estado de humor em indivíduos com epilepsia do lobo temporal (ELT).

Método

Indivíduos com ELT (n = 20) e controles saudáveis (C, n = 20) foram avaliados. Administraram-se questionários para avaliar o estado de humor (POMS) e nível de atividade física habitual (BAECKE). Avaliou-se a aptidão cardiorrespiratória por teste incremental máximo.

Resultados

Pessoas com ELT apresentaram menor aptidão cardiorrespiratória; elevados níveis de transtornos do humor; e menor nível de vigor, quando comparadas ao grupo C. Observou-se correlação negativa significativa entre os níveis de tensão-ansiedade e a potência aeróbica máxima.

Conclusão

O baixo nível de aptidão cardiorrespiratória pode modificar o estado de saúde de indivíduos com ELT e pode ser considerado fator de risco para o desenvolvimento de transtornos de humor.

Palavras-Chave: epilepsia; perfil do estado de humor; POMS; atividade física; exercício; aptidão cardiorrespiratória

Epilepsy is a chronic neurological disorder that leads to a sedentary lifestyle, low physical fitness, and numerous co-morbidities1. Mood disturbances, particularly depression and anxiety, are co-morbidities that have a high incidence in people with epilepsy2,3. Traditionally, pharmacological therapy remains the mainstay of treatment for mood disturbances2. However, non-pharmacological treatments such as physical activity have also been used to reduce mood disturbance levels. In the general population, regular exercise contributes to mood-related benefits4 and minimizes the impact of stressful life events5; similar results have been found in people with epilepsy6,7.

The favorable effects of regular exercise on physical fitness and general health are unquestionable and numerous studies have reported positive effects of regular physical activity in people with epilepsy6,7,8,9,10,11,12. Regular physical activity has been proposed as a positive coping strategy in the management of patients with epilepsy that are diagnosed with mood disorders13,14. Roth et al.15 reported that individuals with epilepsy are more predisposed to mood disorders and that exercise might minimize this predisposition. Recently, de Lima et al.16 reported that the level of physical activity in leisure time can predict mood state disorders in epilepsy. Indeed, the effects of physical exercise on people with epilepsy such as an improvement in psychological health and a decrease in seizure frequency have been increasingly reported in the literature11,12,17. We have previously proposed that physical exercise minimizes mood disorders, particularly depression, in epilepsy12. In this regard, the relationship between physical activity levels and mood disorders may be mediated in part by physiological changes, such as lower levels of maximal aerobic power18,19. Therefore, the aim of the present study was to verify the possible association between cardiorespiratory fitness, habitual physical activity level, and mood state variables in individuals with temporal lobe epilepsy.

METHOD

Participants

Patients with epilepsy were recruited from a Neurological Clinic (Clínica Itapeti, Mogi das Cruzes, Brazil). The epilepsy group consisted of 20 individuals with temporal lobe epilepsy (TLE) and the control group (C) consisted of healthy subjects (recruited from members of the Federal University of Sao Paulo), matched for gender and age with the TLE group. Subjects were informed of the purpose of the study prior to their participation. The TLE and C groups consisted of 11 women and 9 men (n = 20). General characteristics (physical and physical fitness characteristics) of the TLE and C groups are presented in Table 1. The exclusion criteria were any progressive neurological disorders (with the exception of epilepsy) and cognitive limitations. Inclusion criteria were subjects with TLE for at least 2 years and medication compliance. The study was approved by the Federal University of Sao Paulo’s Research Ethics Committee (no. 1845/06) and all participants voluntarily signed informed consent form prior to participating in the study. For individuals younger than 18 years, the participants’ parents signed the informed consent form.

Table 1 Characteristics of C and TLE groups. 

C TLE p-value
N 20 20 N/A
Age (yr) 34.6 ± 11.4 34.1 ± 12.2 0.8604
Height (cm) 167.7 ± 11.3 168.4 ± 11.0 0.6849
Body mass (kg) 69.2 ± 17.3 72.2 ± 17.5 0.871
Body mass index (kg/m2) 24.3 ± 3.5 25.3 ± 5.1 0.636
Physical activity total score (Baecke questionnaire) 7.6 ± 1.3 7.1 ± 1.2 0.2852
Maximal aerobic power (ml/kg/min) 34.4 ± 8.1 28.8 ± 6.7* 0.0361

Data are expressed as mean ± SD. *Statistically significant difference in relation to C (Mann Whitney test, p ≤ 0.05). N/A: Not applicable; C: Control; TLE: Temporal lobe epilepsy.

Study design

Participants from both groups were submitted to the following phases in this order: (1) anamnesis, physical examination, electrocardiogram at rest and during effort, (2) cardiopulmonary exercise test (CPET), and (3) answered the following questionnaires: (a) Profile of Mood States (POMS) and (b) level of habitual physical activity (BAECKE) questionnaire.

Questionnaires

Habitual physical activity questionnaire

The habitual level of physical activity in the C and TLE groups was evaluated by the Baecke questionnaire20. This questionnaire consists of 16 questions involving three habitual physical activity scores (occupational physical activity, physical exercise in leisure time, and leisure and locomotion activities) relating to the previous 12 months. The total score for habitual physical activity was obtained by adding together the cited three habitual physical activity scores. The total scores were recorded for the statistical analysis.

Profile of Mood States Evaluation

The mood profile in the C and TLE groups was assessed by the POMS questionnaire, which is a self-reporting questionnaire consisting of 65 items that fit into 6 categories: tension-anxiety, depression, anger-hostility, vigor, fatigue and confusion, and scored from 1-4 according to severity. The questionnaire yields a global measure of mood. The global score is computed by subtracting the positive category (vigor) from the sum of the five negative categories (tension, depression, anger, fatigue and confusion). The standard instructional set of the POMS questionnaire was employed in this study. The POMS questionnaire was utilized because of its reliability, validity, feasibility and common use in psychometric studies21,22.

Cardiopulmonary exercise test (CPET)

A graded maximal exercise test was administered to the C and TLE groups to determine the maximal oxygen uptake (ml/kg/min). Maximal oxygen uptake is a variable used to assess maximal aerobic power in healthy people and in people with epilepsy23. The subjects were given a standardized set of instructions to explain the test. After these preliminary procedures, each subject was submitted to an incremental maximal exercise test on an air-brake ergometer (Schwinn Airdyne®Exercise Bike, Nautilus Inc, USA). The schedule of this test consisted of a 5-min warm-up at between 10 and 25 watts, followed by progressive load increases at a rate of 10 to 25 watts every two minutes, according to the subject’s cardiorespiratory fitness, until subject exhaustion. Maximal oxygen uptake was always defined as the highest 20-s averaged oxygen uptake value with inclusion criteria consistent with conventional guidelines for maximal oxygen uptake (e.g., an inability to sustain workload, relative HR > 95% age predicted, or respiratory exchange ratio at maximal exercise > 1.1). During the exercise test, subjects were verbally encouraged to exercise for as long as possible. Respiratory gas samples were analyzed breath-by-breath using a gas analyzer (Quark PFT, Cosmed®, Italy). The gas analyzer was calibrated according to the manufacturer's specification prior to each test. Maximal oxygen uptake was recorded for the statistical analyses.

Statistical analysis

Normal distribution and homogeneity of the variances were verified using the Kolmogorov-Smirnov test. The difference between two measures was established by the Mann Whitney test (non-parametric test). To assess possible correlations between maximal aerobic power and total score for habitual physical activity with profile mood states domains we used the Spearman correlation test (alpha ≤ 0.05). Results are presented as mean ± standard deviation (SD). Results were statistically significant at p ≤ 0.05. Statistical analyses were conducted using Graph Pad Prism software (San Diego, CA, USA).

RESULTS

Significant differences were found between the C and TLE groups in maximal oxygen uptake (Table 1). The TLE group presented lower maximal oxygen uptake (28.8 ± 6.7 ml/kg/min) compared with the C group (34.4 ± 8.1 ml/kg/min) (p = 0.0361). The Mann Whitney test revealed differences between the groups for different mood state domains. In the TLE group, the levels of tension-anxiety and confusion (48.2%, p = 0.0223 and 64.8%, p = 0.0274 respectively) were significantly higher compared to the C group. The level of vigor in the TLE group was 16.2% lower (p = 0.0223) compared to the C group. Furthermore, the mood disturbance total score was 83.7% higher in the TLE group (p = 0.0223) compared to the C group (Table 2). Spearman’s correlation analysis (Table 3) showed a significant association between the tension-anxiety domain of the POMS questionnaire and maximal oxygen uptake (p = 0.0460, r = -0.31).

Table 2 Comparison of C and TLE groups on the Profile of Mood States (POMS) scores domains. 

C (n = 20) TLE (n = 20) Effect size p-value
Tension-anxiety 4.5 ± 5.4 8.7 ± 5.5* -0.36 0.0223
Depression 5.6 ± 6.2 10.6 ± 13.0 -0.24 0.1938
Anger-hostility 6.3 ± 6.8 10.6 ± 8.0 -0.28 0.0547
Vigor 19.7 ± 5.4 16.5 ± 4.8* 0.30 0.0482
Fatigue 6.1 ± 5.1 9.1 ± 6.1 -0.25 0.0933
Confusion 1.3 ± 4.6 3.7 ± 4.5* -0.25 0.0274
Disturbance mood total score 4.2 ± 24.6 25.8 ± 34.7* -0.33 0.0315

Data are expressed as mean ± SD. *Statistically significant difference in relation to C (Mann Whitney test, p ≤ 0.05). POMS: Profile of mood state; C: Control; TLE: Temporal lobe epilepsy.

Table 3 Spearman correlation coefficients (number of XY pairs = 40) of the association between POMS scores domains and maximal aerobic power and physical activity total score (Baecke questionnaire). 

POMS scores domains r-value (maximal aerobic power) p-value r-value (physical activity total score) p-value
Tension-anxiety -0.31 0.0460* -0.08 0.5911
Depression -0.18 0.2613 0.01 0.9335
Anger-hostility -0.31 0.0507 -0.17 0.2729
Vigor 0.05 0.7627 0.27 0.0907
Fatigue -0.23 0.1411 -0.13 0.4267
Confusion -0.09 0.5615 0.06 0.6875
Disturbance mood total score -0.24 0.1350 -0.09 0.5807

*Statistically significant correlation (Spearman coefficient, alpha ≤ 0.05).

DISCUSSION

We examined the habitual physical activity levels, cardiorespiratory fitness, the level of mood disorders, and subsequently the impact (correlations) of physical fitness (physical activity levels and maximal aerobic power) on the prevalence of mood disorders in individuals with TLE. Our data showed that people with TLE presented lower levels of cardiorespiratory fitness than healthy subjects. In addition, when compared to healthy subjects, individuals with TLE presented higher levels of mood disorders (tension/anxiety and confusion) and lower levels of vigor/disposition. The present investigation also demonstrates a weak but significant correlation between the levels of tension/anxiety and maximal oxygen uptake, i.e. the lower the levels of cardiorespiratory fitness the higher the levels of tension/anxiety.

Mood and behavioral disturbances are common in epilepsy2,3,24 and have a negative effect on health status and quality of life3. It is important to note that regular physical activity is a non-pharmacological therapy which can provide health benefits such as reduction in the risk of cardiovascular and endocrine diseases, improvement in bone and muscle conditioning25, and prevention of psychological and emotional disturbances10,15,17,26. Consistent with this, mood disturbances are more prevalent among sedentary rather than physically active individuals27. In this regard, Roth et al.15 analyzed the effect of physical activity on depression levels in adults with epilepsy and found that active individuals were less depressed compared to sedentary individuals. Recently, de Lima et al.16 demonstrated that people with juvenile myoclonic epilepsy presented higher levels of mood disturbances when compared to healthy subjects. They showed that the level of physical activity in leisure time predicted 31% of depression levels and 26% of anxiety levels in epilepsy. These data suggest that low levels of physical activity may be considered a risk factor for the development of mood disorders and can play an important role in the global health status of individuals with epilepsy.

It has been reported in healthy subjects that lower levels of physical activity are associated with a greater presence of medical co-morbidities and social isolation26. In support of these findings, Vancini et al.23demonstrated that individuals with TLE presented significantly lower levels of physical activity during leisure time (14.8%) and lower and poorer emotional well-being (17.3%) when compared to healthy subjects. These differences may be associated with the social isolation commonly observed in people with epilepsy28,29. Similarly, Nakken et al.9 observed that a 4-week exercise program improved the mental state and sociability of people with epilepsy. Furthermore, a regular exercise program improved performance and psychosocial quality of life of women with refractory epilepsy10. An improvement in the mood of individuals with epilepsy after 12 weeks of physical training has also been demonstrated by McAuley and collaborators17.

Given the positive contribution of physical activity towards epilepsy, it is reasonable to suggest that physical exercise intervention shows strong positive potential and may be used in an integrated approach in the complementary treatment of epilepsy12. In fact, efforts to promote knowledge about epilepsy and physical activity between health professionals are urgently needed to avoid prejudice in epilepsy treatment and to improve the quality of life and health status of epilepsy patients30. Since physical exercise can exert a positive impact on psychological state and seizure control12, it is desirable that health professionals should recommend and encourage physical exercise programs for people with epilepsy. To this end, we propose that regular physical exercise can be a remarkably positive coping strategy in the treatment of psychological and mood disorders in people with epilepsy12,13. Finally, appropriate management by health professionals of mood states using physical activity can contribute to and positively influence the perceptions of this population of their quality of life and health status.

Acknowledgements

We would like to thank all of the subjects who volunteered their time to participate in this study.

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Support: This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Instituto Nacional de Neurociência Translacional (INNT) (Brazil) and FAPESP-MCT/CNPq-PRONEX.

Received: July 08, 2014; Revised: September 16, 2014; Accepted: October 06, 2014

Correspondence: Ricardo Mario Arida; Departamento de Fisiologia, Universidade Federal de São Paulo; Rua Botucatu, 862 / 5° andar / Ed. Ciências Biomédicas, Vila Clementino; 04023-900 São Paulo SP, Brasil; E-mail: arida.nexp@epm.br

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