Keywords:
Epilepsy, temporal lobe - quality of life - spirituality
Palavras-chave:
Epilepsia do lobo temporal - qualidade de vida - espiritualidade
Religiosity and spirituality are widely regarded as important allies against illness
and suffering in general. Currently, there is an increasing consensus on the importance
of these factors for patients' quality of life[1],[2],[3].
Religiosity can be defined as the degree of participation or adherence in which individuals
believe, follow and practice a religion. It represents the extent of one's faith in
the existence of a supernatural power they believe imbued them with a spiritual nature
that continues to exist after death[1],[2],[3],[4]. Spirituality, in turn, is seen as a human propensity to search for significance
in life; it is a dynamic, personal, and experiential process, often addressed within
the practice of a religious creed, and includes transcendence, purpose, and values
that can be shared by people of different ethnic origins, cultures and religions[1],[2],[3],[5].
Previous studies among temporal lobe epilepsy (TLE) patients suggested that the temporal
lobe could be the main anatomical processing center responsible for individuals' religiosity[6],[7],[8]. Religiosity and spirituality (R/S) can be relevant in patients with epilepsy (PWE)
since their condition can lead to psychosocial issues for many patients and their
families[9],[10],[11],[12],[13],[14].
Therefore, the purpose of this study is the investigation of R/S in PWE and within
different epilepsy syndromes, the underlying hypothesis being that PWE, in particular
with TLE, would have a distinct R/S profile compared with healthy controls.
METHODS
Subjects and structure of study
An observational case-control study was conducted between August 2016 and March 2017
and 150 subjects were included. Of these, 100 consecutive patients had a definite
diagnosis of epilepsy according to the International League Against Epilepsy (ILAE) criteria[9],[15]. The diagnosis was based on clinical history and seizure semiology supported by
electroencephalography (EEG) or video-EEG and magnetic resonance imaging (MRI) or
computed tomography (CT) findings consistent with the diagnosis. All patients were
on treatment with one or more standard antiepileptic drugs (AEDs). They were followed
at the University Hospital of the Federal University of Santa Catarina (UFSC) Epilepsy
Clinic for at least one year. The control group comprised 50 consecutive healthy volunteers
matched for age, sex and educational level, recruited during the same period from
the local community. The following exclusion criteria were adopted:
-
Individuals younger than 18 years;
-
Subjects with intellectual impairment that prevented them from understanding the questionnaires
and the interview;
-
Subjects with either medical or surgical treatment resulting in complete seizure control
for at least one year;
-
Subjects with psychogenic nonepileptic seizures.
Procedure
-
Patients were face-to-face interviewed for sociodemographic data (age, sex, occupation,
marital status, schooling, socioeconomic status) and clinical data (age at onset,
type and frequency of seizures, duration of epilepsy, AEDs and epileptic syndrome).
-
The patients' socioeconomic status was measured using the ABEP's (Brazilian Market
Research Association) questionnaire for socioeconomic stratification criteria updated
for 2016. This instrument attributes different relative socioeconomic classifications
to individuals based on access to basic utilities, material possessions, and level
of education[16].
-
Application of the Index of Core Spiritual Experience (INSPIRIT-R)[17] for quantification of R/S. This instrument contains seven items, the seventh consisting
of a list of 12 types of religious experiences, on which the patient is asked whether
he/she experienced any of them and, if so, whether or not this strengthened his/her
belief in God, and/or convinced him/her of God's existence. Responses were recorded
on a 1-4 scale. Higher scores indicate higher R/S.
-
Application of the Hospital Anxiety and Depression Scale (HADS)[18] to determine anxiety and depression. This scale has 14 items, seven of which are
for anxiety assessment (HADS-A) and seven for depression (HADS-D). After calculating
the score of each sub-scale (0-21), both were summed up in order to obtain the total
score (0-42). Scores over 7 in each sub-scale indicate anxiety or depression.
-
Application of the Quality of Life in Epilepsy Inventory (QOLIE-31)[19],[20] to determine quality of life. This is a globally used epilepsy-specific instrument
with seven domains: worry about seizures, overall quality of life, emotional well-being,
energy–fatigue, cognitive functioning, medication effects, and social functioning.
The overall score ranges from 1 to 100. Higher scores indicate higher quality of life.
The PWE were tested with all the above procedures, and the control group (CG) with
procedures 1, 2, and 3. These instruments have been previously validated in Brazil[21],[22],[23].
Data analysis
Statistical analysis was performed using GNU PSPP® for Windows, STATISTICA® Ultimate Academic version, and Microsoft Excel® software package for Windows, 2014. Descriptive analysis was made to characterize
the sample. Quantitative variables were expressed as mean ± standard deviation (SD)
and qualitative variables were expressed as frequency and percentage values. Two-tailed
Student's t-test was applied to compare continuous variables, while Fisher's exact
test (2 x 2 contingency tables) or Pearson's Chi square analysis (3 x 2 contingency
tables) was used to compare qualitative data and frequencies of occurrence. A p-value
< 0.05 was considered to be statistically significant.
Ethics
This study was carried out in accordance with the Code of Ethics of the World Medical
Association (Declaration of Helsinki) and was only started after approval by the UFSC
Ethics Committee for Human Research[24]. All subjects signed an informed consent form and voluntarily agreed to participate.
RESULTS
Sociodemographic variables for patients and controls are listed in [Table 1]. The patients' age ranged from 18 to 66 years, similar to the controls, who had
an age range of 19-83 years. Although PWE and controls had similar years of schooling,
they differed with regard to socioeconomic status, in which most patients were in
ABEP class C, while the majority of controls were in class B.
Table 1
Sociodemographic characteristics of participants.
|
Sociodemographic variables
|
PWE (n = 100)
|
Controls (n = 50)
|
p-value
|
|
Sex
|
|
Male
|
45 (45.0%)
|
16 (32.0%)
|
0.128
|
|
Female
|
55 (55.0%)
|
34 (68.0%)
|
|
Age, mean ± SD
|
35.9 ± 12.4
|
36.3 ± 18.1
|
0.894
|
|
Years of schooling, mean ± SD
|
8.9 ± 3.7
|
10.1 ± 4.2
|
0.081
|
|
Education level
|
|
Incomplete Elementary School
|
30 (30.0%)
|
13 (26.0%)
|
|
|
Complete Elementary School
|
12 (12.0%)
|
1 (2.0%)
|
|
|
Incomplete High School
|
9 (9.0%)
|
3 (6.0%)
|
0.051
|
|
Complete High School
|
30 (30.0%)
|
10 (20.0%)
|
|
Incomplete Superior Education
|
12 (12.0%)
|
22 (44.0%)
|
|
|
Complete Superior Education
|
7 (7.0%)
|
1 (2.0%)
|
|
|
Socioeconomic status*
|
|
A
|
3 (3.0%)
|
3 (6.0%)
|
|
|
B
|
32 (32.0%)
|
26 (52.0%)
|
0.007**
|
|
C
|
58 (58.0%)
|
20 (40.0%)
|
|
D/E
|
7 (7.0%)
|
1 (2.0%)
|
|
PWE: patients with epilepsy; SD: standard deviation;
*ABEP socioeconomic stratification criteria updated for 2016; patients and controls
were not paired with regard to socioeconomic status.
**Statistically significant p value.
PWE had an average age of disease onset during adolescence and a mean of two decades
of epilepsy duration, the majority of patients were using two AEDs, and an average
monthly frequency of epileptic seizures of 5.9 ± 12.6.
In terms of the different epilepsy syndromes, 72% of patients had focal epilepsies,
mainly (63%) with TLE. The remaining included patients with idiopathic generalized epilepsies and some cases
not clearly belonging to any definite syndrome. For statistical analysis, they were
grouped together with the focal extratemporal epilepsies as “other”.
With regard to R/S, PWE had similar INSPIRIT-R scores to the controls, with both groups
having an average of 3.1 on a scale that quantitatively estimates R/S ranging from
1 (minimum R/S) to 4 (maximum R/S). Comparing TLE patients with other PWE and controls,
the TLE group had a higher score on the INSPIRIT, which demonstrates a quantitatively
higher degree of R/S ([Table 2]).
Table 2
Participants' scores in scales/questionnaires.
|
Variables
|
INSPIRIT-R
|
HADS
|
QOLIE-31
|
|
Mean ± SD
|
p-value
|
Mean ± SD
|
p-value
|
Mean ± SD
|
p-value
|
|
Control (n = 50)
|
3.1 ± 0.8
|
0.904
|
12.6 ± 6.6
|
0.422
|
–––
|
–––
|
|
PWE (n = 100)
|
3.1 ± 0.8
|
|
13.6 ± 7.7
|
|
–––
|
–––
|
|
TLE (n = 63)
|
3.3 ± 0.7
|
0.041*
|
13.5 ± 7.9
|
0.776
|
58.4 ± 16.1
|
0.755
|
|
Other (n = 37)
|
2.9 ± 0.9
|
|
13.9 ± 7.6
|
|
59.7 ± 20.7
|
|
PWE: patients with epilepsy; SD: standard deviation; TLE: temporal lobe epilepsy.
*Statistically significant p value.
Upon analyzing quality of life in PWE, those with TLE achieved similar scores to those
of patients with other epilepsies on the QOLIE-31 scale, as shown in [Table 2].
Anxiety and depression scores on the HADS scale showed no statistically significant
difference between PWE and controls, though scores for the PWE group appeared slightly
higher. Regarding epilepsy subtypes, patients with TLE likewise scored slightly lower
for anxiety and depression, but the difference was not statistically significant ([Table 2]).
In terms of correlation between R/S scores and clinical-demographic variables ([Table 3]), in the control group no statistically significant correlation was found between
the degree of R/S, age and years of schooling. In the epilepsy group, however, there
was a statistically significant correlation between R/S and age, such that older patients
had higher R/S. There was also a significant correlation between R/S in PWE and total
years with epilepsy, such that patients living with epilepsy for a longer period had
higher R/S. There was no correlation between R/S and years of schooling, number of
AEDs in use and monthly frequency of epileptic seizures in PWE.
Table 3
Correlations - scores/scales vs. clinical-demographical variables.
|
Variables
|
INSPIRIT-R
|
HADS
|
QOLIE-31
|
|
r
|
p-value
|
r
|
p-value
|
r
|
p-value
|
|
PWE
|
|
Age
|
+0.32
|
0.001*
|
+0.06
|
0.570
|
-0.07
|
0.500
|
|
Schooling (years)
|
-0.04
|
0.720
|
+0.06
|
0.559
|
-0.11
|
0.279
|
|
Number of AEDs
|
+0.06
|
0.571
|
+0.13
|
0.203
|
-0.08
|
0.431
|
|
Duration of epilepsy
|
+0.25
|
0.011*
|
+0.06
|
0.542
|
-0.07
|
0.510
|
|
Seizure frequency (per month)
|
+0.04
|
0.754
|
+0.08
|
0.528
|
-0.18
|
0.129
|
|
Controls
|
|
Age
|
+0.21
|
0.151
|
-0.35
|
0.011*
|
–––
|
–––
|
|
Schooling (years)
|
-0.16
|
0.275
|
+0.28
|
<0.001*
|
–––
|
–––
|
AEDs: antiepileptic drugs; PWE: patients with epilepsy; r: Pearson's correlation coefficient;
*Statistically significant p-value.
Correlations between scales/scores of R/S, quality of life and anxiety and depression
are shown in [Table 4]. Although there were no significant correlations between the INSPIRIT-R scale and
HADS or QOLIE-31, there was a negative correlation between HADS and QOLIE-31 in PWE,
suggesting that patients with more anxiety and depression have lower quality of life.
Table 4
Correlations between scores/scales.
|
Scores/Scales
|
r
|
p-value
|
|
PWE
|
|
INSPIRIT-R vs. HADS
|
+0.07
|
0.457
|
|
INSPIRIT-R vs. QOLIE-31
|
+0.07
|
0.507
|
|
Controls
|
|
HADS vs. QOLIE-31
|
-0.65
|
< 0.001*
|
|
INSPIRIT-R vs. HADS
|
-0.12
|
0.410
|
PWE: patients with epilepsy; r: Pearson's correlation coefficient;
*Statistically significant p value.
DISCUSSION
R/S in patients with epilepsy compared with controls
INSPIRIT-R means were similar between PWE and healthy controls. This could be due
to the already considerably high levels of R/S found in the Brazilian population that
could obfuscate minor differences between different population subsets. In a recent
transcultural study of locus of control in PWE comparing Brazilians and Lithuanians,
the INSPIRIT-R scores differed strongly (3.11 ± 0.87 vs. 2.45 ± 0.72, p < 0.0001),
in Lithuania likewise without significant difference from healthy controls[25].
Our results deviate from the previous literature, which compared only measures of
religiosity between epilepsy and control groups, without consideration to the wider
context of spirituality. Tedrus et al. found that PWE (n = 159) had a higher health-related
religiosity score when compared to a control group (n = 50) using the Duke Religion
Index[26]. This instrument, however, limits the variable of religiosity, assessing it purely
as pertaining to health. Notwithstanding this, Tedrus et al., in another study, did
not find a significant association between spirituality in PWE (n = 196) when compared
with controls (n = 66), corroborating our findings[27].
R/S and the temporal lobe
In a comparative analysis between TLE and other epilepsies, we found R/S means that
were significantly higher in the TLE group, supporting the hypothesis that the temporal
lobe could be the main anatomical processing center responsible for individuals' religiosity[6],[7],[8].
R/S and social-demographic factors
No correlation was found between INSPIRIT-R, age and years of schooling within the
controls, which suggests that those variables should not influence general individuals'
R/S. In the epilepsy group, however, older patients had higher R/S, while years of
schooling did not correlate with R/S. These findings disagree with those of Tedrus
et al., also undertaken in Brazil, which suggest that spirituality in PWE is associated
with fewer years of schooling[27].
R/S and clinical factors in epilepsy
Patients with longer duration of epilepsy had higher scores on INSPIRIT-R. As the
correlation between age and INSPIRIT-R was not observed in the controls, our finding
may evidence some form of disease-related coping. It happens when people turn to R/S
as a means of dealing with stress or problems in general. Depending on the way it
is used, coping can be both positive – for example, when someone draws upon faith
for resilience in the face of an obstacle in life – or negative – when one justifies
their suffering as being warranted in light of some divine punishment. Tedrus et al.
also found significant associations between coping and clinical aspects of epilepsy:
while disease duration was associated with positive coping, frequency of seizures
and earlier disease onset were both associated with negative coping mechanisms[5].
In that vein, PWE in our study are probably using positive forms of coping as long
as their disease is active, facing epilepsy as a barrier that must be overcome. Health
professionals need to consider R/S, as well as the coping mechanisms derived from
it, as potential factors to foster appropriate intervention on epilepsy care. In some
PWE with higher R/S – especially among older ones and those with longer histories
of epilepsy – negative coping strategies might be more prevalent, possibly interfering
in patients' treatment response[14].
R/S and quality of life
INSPIRIT-R scores were not correlated with QOLIE-31, but PWE with lower levels of
anxiety and/or depression had better scores on QOLIE-31. Additionally, patients with
TLE obtained similar scores as those with other epilepsy subtypes on the QOLIE-31
scale.
A recent study undertaken in South Korea with 232 PWE found that lower levels of religiosity
were linked to increased levels of anxiety and depression. However, this study again
did not take into consideration the component of spirituality. Furthermore, the study
evaluated high-functioning PWE, given that 85% of them had a high school level of
education (versus only 49% from our sample). As such, their findings might not be
readily generalizable to PWE in most developing countries[28].
Giovagnoli et al. found an association between spirituality and quality of life in
patients with focal epilepsy[29]. These results, however, were obtained comparing patients with different epilepsy
subtypes in an attempt to explain their findings of PWE of similar severity, without
comparison to control groups.
Finally, Tedrus et al. recently conducted a study in Brazil with 209 individuals (159
with epilepsy and 50 controls) in which – like in our study – no association was found
between R/S and quality of life[26].
Limitations and future perspectives
This study compared R/S quantitatively between individuals with and without epilepsy.
Patients' specific religious denominations, however, were not considered. Future studies
should search for distinctions between different religions' performances on the INSPIRIT-R.
In addition, the group of “other epilepsies” is a rather heterogeneous pool including
subgroups that were too small to be analyzed separately but for which different relations
could exist.
Specific religious and/or spiritual experiences patients might have had during (ictal),
after (postictal) or in between (interictal) seizures were not explored in this study.
Despite controversy in using epilepsy as a model to explain such experiences, a recent
review of the literature points to TLE as having an important influence on religious
and literature history, given that a considerable number of important religious figures
including prophets, saints and even cult founders have had experiences very much akin
to those of modern-day patients suffering from seizures in TLE[30]. Religious connotations – such as seizures being described as a punishment for sins,
or even being considered a sign of prophetic abilities – are a primordial constituent
part of the sociocultural context of epilepsy and can be observed in literature by
means of religious metaphors[31]. There is also a growing body of clinical and historical evidence dating back 150
years linking epilepsy in general to religious experiences in patients in ictal, postictal
and interictal states[32].
Although this study found significant associations between R/S and TLE, further research
is needed with larger cohorts to identify the impact of R/S on physical and mental
health and to determine how these variables could influence clinical outcomes and
quality of life in PWE.
In conclusion, there were no differences on R/S of PWE compared with controls; TLE
patients, however, were found to have higher levels of religiosity and spirituality
than PWE with other epilepsy subtypes, supporting the theory that the temporal lobe
could be structurally or physiologically associated with the experience of religiosity
and spirituality in the human mind.
