postpoliomyelitis syndrome - poliomyelitis - energy metabolism
síndrome pós-poliomielite - poliomielite - metabolismo energético
The post-poliomyelitis syndrome (PPS) is a late effect of poliomyelitis, classified
as motor neuronopathy, since the clinical and histological aspects are closely related
to dysfunction of the lower motor neurons[1]. The frequency of PPS varies from 22% to 80% in different international studies.
A Brazilian study showed a frequency of 77,2% in patients classified as having PPS,
of which 62.8% were women and 37.2% were men[2].
The PPS usually occurs 30-50 years after the acute polio infection. It is characterized
by new symptoms or worsening of previous residual symptoms such as: new weakness,
muscle fatigue, new atrophy, muscle pain, joint pain and cold intolerance[3],[4],[5],[6]. Currently, it is recognized as a disease entity defined by the World Health Organization,
and is represented in the International Code of Disorders (ICD10/G14)[7].
Different hypotheses have been proposed for the pathophysiology of PPS[8],[9],[10],[11], but the most accepted is the theory of “overuse” (overload or overtraining), proposed
by Charcot[12] and defended by others[13],[14],[15],[16].
The most important characteristic of PPS is the development of a new muscle weakness.
This new weakness may occur in muscles that already have some degree of muscle weakness
or muscles that were previously committed, and subsequently reinnervated. This new
weakness inevitably leads to increased energy expenditure for the performance of routine
physical activity[17].
Some risk factors, such as age, gender, severity of paralysis, pain, intensity of
muscular exercise, or physical activity[18],[19] may contribute to the development of PPS. Possible relationships between these factors
and energy metabolism are of paramount importance[20].
Different methods are used for the subjective assessment of habitual physical activity;
most of them are represented by questionnaires coming from epidemiological studies[21]. Assessment of physical activity by questionnaire is a method that is influenced
mainly by the ability of people to recall[22].
The Baecke questionnaire for the evaluation of habitual physical activity[23], is a recall instrument that is easy to apply and understand; it is a qualitative-quantitative
scale and addresses aspects such as occupational physical activity, physical exercise
in leisure and activities in leisure and locomotion. This instrument has been used
in epidemiological study in the Brazilian population[24].
The objective of this study was to identify energy expenditure, retrospectively, in
individuals with PPS in the Brazilian population, and verify whether physical activity
may be a predisposing factor for the development of PPS, or worsening of the patient’s
symptoms.
METHODS
Three distinct groups of individuals were evaluated: poliomyelitis sequelae (PS),
PPS, and a control group (CG). The population of interest comprised patients with
a history of paralytic poliomyelitis who underwent ambulatory monitoring in the Neuromuscular
Disorders Unit, at the Federal University of Sao Paulo (UNIFESP), in the municipality
of Sao Paulo, Brazil, and healthy individuals (caregivers of patients), between the
years 2007-2009.
The inclusion criteria were male and female patients with a confirmed diagnosis of
paralytic polio and PPS. Patients older than 60 years and the presence of any disease
or medical condition that could lead to muscle weakness were excluded. This study
was approved by the Ethics Committee of UNIFESP and all patients involved in the study
agreed and signed the informed consent form.
To evaluate habitual physical activity, we used the Baecke questionnaire[23], which had been translated and validated into Portuguese by Florindo and Latorre[24].
The Baecke encompasses three levels of physical activity characterized by occupational
physical activity (questions 1–8), physical exercise and leisure activities (questions
9–12), and physical leisure and locomotion activities (questions 13–16), all of which
comprise the assessment of habitual physical activity. The total score (TS) is the
sum of the scores of these three levels. Formulae to calculate the Baecke questionnaire
were:
TS = OPA+PEL+LLA
vq = value of the question
OPA = occupational physical activity
PEL = physical exercises in leisure
LLA = physical leisure and locomotion activities
TS = total score
The Baecke questionnaire was applied to the three groups (PS, PPS and CG) just once,
assessing the history of physical activity throughout life in periods at 10-20 years
of age, 21–30 years of age and in the last 12 months, excluding the occupational activities
in the period from 10–20 years, resulting in nine final scores of the respective periods
([Figure 1]).
Figure 1 Methodology to apply the questionnaires.
For the classification of the energy expenditure of occupational physical activity
and the types of exercise that were not in the standardization profile[23], we used the studies by Ainsworth et al.[25] and McArdle et al.[26] as reference. The first study was a coding scheme for the classification of energy
cost of human physical activities, and the latter proposed levels of classifications
of human energy expenditure of physical activity (based on a multiple of the resting
metabolic rate).
For fatigue evaluation, we use the Fatigue Severity Scale[27]. It consists of nine items. Individuals record their responses from 1–7 (1 means
that they disagree completely and 7 indicates that they fully agree with the statement).
This scale assesses the complaint of fatigue in the previous two weeks.
We also used the abbreviated World Health Organization Quality of Life assessment
tool[28]. This questionnaire has 26 questions, the first two are general and the other 24
divided into four domains: physical (dom 1), psychological (dom 2), social relationships
(dom 3), environment (dom 4) and overall. Steps for checking and cleaning data and
computing facet and domain scores were:
Recode q3 q4 q26 (1=5) (2=4) (3=3) (4=2) (5=1).
compute dom 1 = (mean.6 (q3, q4, q10, q15, q16, q17, q18)) * 4.
compute dom 2 = (mean.5 (q5, q6, q7, q11, q19, q26)) * 4
compute dom 3 = (mean.2 (q20,q21,q22)) * 4
compute dom 4 = (mean.6 (q8, q9, q12, q13, q14, q23, q24, q25)) * 4
compute overall = (mean.2 (q1, q2)) * 4
Analyses were performed by PRISM 3 software, by comparing their percentage by category,
calculation of mean, median and standard deviation.
Continuous variables with normal distribution were tested by the Kolmogorov-Smirnov
test.
Analysis of variance (ANOVA) was used to compare the groups when presented with parametric
data. When statistically significant differences were found, the analysis was complemented
by Tukey’s test.
Analysis of variance (Kruskall-Wallis) was used to compare the groups when presented
with non-parametric data. When statistically significant differences were found, analysis
was complemented by Dunn’s test.
Evaluation of linear correlation was made using the Spearman’s (r) correlation coefficient.
For all tests, results were considered statistically significant when p < 0.05.
RESULTS
One hundred and sixteen individuals participated in the study, 52 with PPS, 28 with
PS and 36 in the CG. The gender distribution of the CG was 19 women (52.7%) and 17
men (47.3%); in the PS group: 17 women (60.7%) and 11 men (39.3%); and in the PPS
group there were 26 women (50%) and 26 men (50%).
The average age for each group was: 42.86 ± 9.22 years for the CG; 43.31 ± 6.91 years
for the PS group; and 43.83 ± 6.65 years for the PPS group (ranging from 30 to 59
years). Measures of central tendency and dispersion for anthropometric variables,
assessed by group, are presented in [Table 1].
Table 1
Mean values and standard deviations of the anthropometric characteristics of the groups
involved in the study.
|
Variable
|
CG (n = 36)
|
PS (n = 28)
|
PPS (n = 52)
|
|
Height (cm)
|
170.5 ± 10.9*
|
161.2 ± 8.0
|
163.4 ± 10.3
|
|
Weight (Kg)
|
74.6 ± 17.6
|
62.7 ± 15.8**
|
68.7 ± 15.4
|
|
BMI (Kg/m2)
|
25.5 ± 4.1
|
23.8 ± 4.9
|
25.5 ± 4.1
|
Test ANOVA (one way analysis of variance); *p = 0,0007 vs PS and PPS; **p = 0,0124
vs CG.
CG: control group; PS: poliomyelitis sequelae; PPS: post-poliomyelitis syndrome; BMI:
body mass index.
The lowest age at which acute poliomyelitis occurred was 23 days and the highest was
eight years; the average was 19.71 months (one year and seven months), with a standard
deviation of 16.8 months (1.4 years), and the median was 18 months (nine and 24 months).
The average age of onset of new symptoms of PPS was 37.7 ± 6.3 years (24-53 years).
On the Fatigue Severity Scale, there was a significant difference (p < 0.0001) between
the CG (17.56 ± 11.4), the PS group (27.29 ± 20.5) and PPS group (51.48 ± 14.21).
The PPS group showed higher fatigue scores, with 92.3% of patients being classified
with fatigue. In contrast, in the PS and PPS groups, there was no relationship between
fatigue and other criteria evaluated in this study (demographic, anthropometric, history
of poliomyelitis, quality of life and energy expenditure).
The group of patients with PPS showed an index of quality of life significantly worse
in the physical, psychological and environment domains, when compared with the other
groups (CG and PS). There was no difference in the social networking domain ([Table 2]).
Table 2
Classification of scores for each group of domains of WHOQOL-Bref.
|
Dominion WHOQOL
|
CG (n = 36)
|
PS (n = 28)
|
PPS (n = 52)
|
p-value
|
|
Physical
|
75.9 ± 14.3
|
67.9 ± 17.1
|
42.4 ± 16.5
|
< 0.0001a
|
|
Psychological
|
73.6 ± 13.4
|
73.5 ± 15.6
|
59.3 ± 16.9
|
< 0.0001b
|
|
Social relationships
|
74.6 ± 20.5
|
72.7 ± 21.1
|
67.8 ± 18.5
|
(ns) 0.128
|
|
Environment
|
66.1 ± 17.5
|
62.7 ± 17.0
|
56.7 ± 15.7
|
= 0.0312c
|
Test ANOVA (one way analysis of variance) with Tukey’s post-test, significant difference:
agroup PPS vs PS and CG;bgroup PPS vs PS and GC; cgroup PPS vs CG. CG: control group;
PS: poliomyelitis sequelae; PPS: post-poliomyelitis syndrome; WHOQOL: World Health
Organization Quality of Life scale.
The PPS group showed an increase in energy expenditure in their occupational activities
(professional), compared to the PS group in the period from 21 to 30 years of age
([Figure 2]).
Figure 2 Longitudinal comparison of the period from 21 to 30 years of age between CG, PS and
PPS of OPA score.*p < 0,05 vs PS (Test Kruskal-Wallis). CG: control group; PS: poliomyelitis
sequelae; PPS: post-poliomyelitis syndrome; OPA: occupational physical activity.
Occupational physical activity between 21 and 30 years of age showed correlations
with other variables in the survey ([Table 3]).
Table 3
Spearman’s correlation coefficients and p values between occupational physical activity
(21 to 30 years of age) and the variables years of study, acute polio and age of onset
of new symptoms.
|
Variables
|
Correlation coefficients (r)
|
p-value
|
|
Education (years of study)
|
- 0.3720
|
0.0066
|
|
Acute poliomyelitis
|
- 0.2803
|
0.0390
|
|
Age at onset of PPS
|
- 0.2796
|
< 0.0447
|
The [Figure 3] shows that the PPS group, during the evaluation of physical activity performed in
the previous 12 months, had a lower energy expenditure in all scores of the Baecke
Questionnaire of Habitual Physical Activity, in relation to the PS and CG.
Figure 3 Longitudinal comparison of the period from last 12 months between CG, PS and PPS
of OPA, PEL, LLA and Total Score (TS). All analyses were performed using the Kruskal-Wallis:
*p < 0.05 vs PS and GC.CG: control group; PS: poliomyelitis sequelae; PPS: post-poliomyelitis
syndrome; OPA: occupational physical activity; PEL: physical exercises in leisure;
LLA: physical leisure and locomotion activities; TS: total score.
DISCUSSION
The aim of this study was to describe the profile of energy expenditure using the
Baecke Questionnaire of Habitual Physical Activity, showing the relationship between
habitual physical activity and the development of symptoms of PPS. In this study,
it was important to assess whether physical activity may be a predisposing factor
for the development of PPS, or worsening of their symptoms.
Fatigue has been found with high frequency affecting, on average, two-thirds of patients
with PPS. This finding can be seen both in studies in the United States[29] and in other Brazilian studies[2],[30]. The study by Conde et al.[30] showed that fatigue in patients with PPS is not related to time of day (morning
or evening) but with the type of activity. In our research we analyzed the history
of physical activity, professions and sports practiced and did not find any relationship
with the variable of fatigue. This could be explained by two hypotheses: fatigue is
an independent symptom that deserves specific management; or fatigue is not a good
marker of PPS.
Patients with PPS were found to have a poor quality of life compared to the PS and
CG groups, mainly in the physical, psychological and environmental domains. The presentation
of new symptoms alone, is likely to lead to an impaired quality of life compared to
the other groups.
The three groups (CG, PS and PPS) showed a gradual and significant increase in scores
of occupational physical activity and total scores over the three periods analyzed.
But there was a gradual and significant decrease over the years in physical activity
scores in leisure, and physical activity in leisure and locomotion, most likely due
to changes in lifestyle, resulting in inactivity in leisure sporting practices.
However, in studied clinical period (previous 12 months), clinical worsening in the
patients with PPS may explain why they could not perform activities of leisure, as
opposed to lack of opportunity, lack of desire or pleasure linked to another factor.
Both the PS and PPS group had a history of sequelae and physical disabilities, but
only the PPS group showed a significant decrease in all their habitual physical activities
(occupational physical activity, physical exercise and leisure and locomotion activities,
and total scores) in the previous 12 months.
On the other hand, patients with PPS had a higher energy expenditure in occupational
physical activity, in the period from 21 to 30 years of age, which was the only factor
that corroborates the hypothesis of “overuse”.
Considering that PPS is a disease with giant motor units, the increased energy expenditure
in any domain of the Baecke questionnaire could indicate an overload in motor units[3].
The PPS group showed a negative correlation between occupational physical activity,
from 21 to 30 years of age, and onset of new symptoms, indicating that the occupational
physical activity (profession) exercised in this period is the factor that provided
the physical overload causing the earlier appearance of new symptoms[13].
The PPS group also showed a negative correlation between occupational physical activity,
from 21 to 30 years of age, and the educational level, indicating that those who performed
more physical activity in their occupation (profession) in this period had a low educational
level. This finding indicates that a high level of education may possibly be a protective
factor for PPS.
The PPS group showed a negative correlation between occupational physical activity,
from 21 to 30 years of age and the age of acute poliomyelitis, indicating that those
who had polio later had less energy expenditure in their occupational activities in
the period. Therefore, the age of the acute poliovirus infection negatively affected
the work performance of patients, corroborating the statement about the severity of
sequelae and physical losses of those patients with PPS.
Because this study was performed in a research center that specialized in neuromuscular
diseases, the search for the patients was passive and spontaneous. The patients evaluated
were those with more symptoms or who had any social and/or legal necessity. However,
even though using a questionnaire as a research tool, which allowed the retrospective
analysis of energy expenditure, the patients in question had no difficulty in understanding
and completing the questionnaire, and this corresponded to a longer period of educational
study (over 15 years of study: PPS = 48%, PS = 28.6% and CG = 33.3).
The study of an energy expenditure profile in individuals with a history of prior
paralytic poliomyelitis showed that the PPS is a nosological condition with its own
characteristics, and the overuse of motor units during life is one of the causal factors;
it is directly linked with the historical expenditure of energy during life; PPS patients
had a higher energy expenditure, especially in occupational physical activity, between
21 and 30 years of age, suggesting that this decade is critical for the development
of this condition; at the present time, patients with PPS have a different status
in relation to the PS and CG groups, with a higher frequency of fatigue, lower scores
on usual physical activities and consequently poorer quality of life; being overweight
can be an aggravating factor for the development or intensification of these limitations.
Considering that PPS may have a relationship with greater physical activity in a given
period of life and/or increased basal metabolism[31], future research is needed to compare the Fatigue Severity Scale with basal metabolic
measures.
