Background
Stroke may affect nutritional status and body composition by causing eating difficulties and reduced mobility [
1]. Nutrition and stroke are closely linked. On one hand, obesity and unhealthy eating habits may contribute to stroke events. On the other hand, post-stroke weight loss and malnutrition are common with reports of varying prevalence related to the characteristics of the examined group [
2]. In one study of a cohort of older stroke individuals, self-reported weight loss of greater than 3 kg was reported in 26 % 1 year after stroke, and more severe stroke incidents were associated with greater weight loss [
3]. Poor food and protein intake may further promote a catabolic state and the progression towards muscle loss and sarcopenia [
4]. Conversely, approximately half (52 %) of the individuals in the previously mentioned population-based cohort were overweight at the time of the stroke, and 61 % were overweight after 1 year [
3].
Alterations in body composition, such as loss of muscle mass and increased fat mass (FM), are part of physiological ageing. Physical inactivity, poor nutrition, chronic diseases, and hormonal changes may contribute to altered body composition [
5]. Sarcopenia is defined as the combination of low muscle mass with low muscle strength and/or function [
6]. Individuals who do not regain walking capacity 1 year after stroke display a 6 % loss of leg lean tissue mass [
7]. Depending on the diagnostic criteria and the cohort characteristics, the reported prevalence of sarcopenia varies between 1 and 30 % and increases with age in the general population [
8]. Hemiparetic stroke in particular may lead to secondary muscle atrophy and specific changes in metabolic and contractile capacity [
9].
The combined state of muscle wasting and obesity is known as sarcopenic obesity (SO) [
9,
10]. The rates of SO in the elderly are reported to be 2 % and 10 % in those < 70 years and > 80 years, respectively [
9]. Although sarcopenia and SO may complicate the post-stroke trajectory [
6,
11], data on the prevalence of these conditions after stroke are sparse.
The aims of this study were to determine the physical function and mobility in relation to nutritional status and body composition, i.e., obesity, sarcopenia, and SO in community-dwelling post-stroke individuals one to 3 years after the stroke incident. We hypothesised that mobility in older individuals who had suffered a stroke would be related to fat-free mass (FFM), nutritional status, and physical activity level.
Results
Table
1 presents the baseline characteristics of the 134 participants. A median of 13 months (range: 12 to 38 months) had elapsed between the stroke event and the post-stroke examination.
Table 1
Characteristics of the included participants (n = 134)
At examination | |
Age, years, mean (SD) | 74 (7) |
Male, n (%) | 93 (69) |
Living alone, n (%) | 35 (26) |
Social support, n (%) | |
Yes, partial | 36 (27) |
Yes, complete | 11 (8) |
At stroke |
Stroke characteristics, n (%) | |
Cerebral infarction | 117 (87) |
Intra-cerebral haemorrhage | 17 (13) |
Thrombolysis, n (%) | 6 (5) |
CCI, n (%) | |
0 | 83 (63) |
1 | 37 (27) |
2 | 12 (9) |
3 | 2 (1) |
Risk factors for stroke, n (%) | |
Earlier stroke | 27 (21) |
Transient Ischemic Attack | 13 (10) |
Diabetes | 20 (16) |
Atrial fibrillation | 28 (22) |
Hypertension | 82 (65) |
Smoking | 18 (14) |
SPMSQ, (0–10 p), median (IQR) | 10 (1) |
Two-thirds of the participants were men, and all were Caucasian. The gender distribution and age were the same among the eligible subjects who did not participate in the study for various reasons (Fig.
1). Cognitive function (SPMSQ) was high; 71 % of the participants had the highest possible score. Among the 61 participants who could not undergo BIA, the gender distribution (74 % males) and age (75 [5.0] years) were similar, whereas the SPPB score (median of 8 points) was reduced (
p < 0.001) and the co-morbidity rate was higher (
p = 0.025) compared with those who underwent BIA.
Data on nutritional status, physical function, body composition, and bio-chemical variables are presented in Table
2. Although MNA-SF indicated a normal nutritional status in general, 14 % were considered at risk for malnutrition. None were malnourished. Overweight was observed in 48 %, and obesity (BMI ≥ 30 kg/m
2) was observed in 22 % of the subjects.
Table 2
Nutritional status body composition, physical function and bio-chemical status, 1–3 years after stroke
MNA-SF (0–14 p), median (IQR)a
| 14 (2) | 14 (1) | 13 (2) | 13 (2) | 13.5 (2) | 0.24 |
BMI (kg/m2), mean (SD) | 27.3 (4.1) | 27.8 (4.0) | 26.4 (2.8) | 27.4 (4.8) | 27 (5.4) | 0.68 |
BMI class, (kg/m2), n (%) | | | | | | |
< 22 | 8 (6) | 3 (5.6) | 1 (2.6) | 2 (8.7) | 2 (11.1) | NA |
22–24.9 | 31 (23.3) | 11 (20.4) | 12 (31.6) | 5 (21.7) | 3 (16.7) | 0.62 |
25–29.9 | 64 (48.1) | 24 (44.4) | 20 (52.6) | 12 (52.2) | 8 (44.4) | 0.17 |
≥ 30 | 30 (22.6) | 16 (29.6) | 5 (13.2) | 4 (17.4) | 5 (27.8) | 0.41 |
10 mWT (m/s), mean (SD) | 1.08 (0.25) | 1.16 (0.25) | 1.10 (0.22) | 0.96 (0.23) | 0.94 (0.23) | >0.001 |
<1.0 m/s, n (%) | 38 (28) | 11 (12) | 7 (7) | 11 (27) | 9 (2) | |
SPPB (0–12 p), median (IQR) | 10 (3) | 11 (16) | 10 (4) | 10 (3) | 9 (4) | 0.005 |
≤ 8, n (%) | 37 (41) | 15 (16) | 19 (20) | 10 (24) | 11 (27) | |
PASE, (0 ≤ p), mean (SD) | 108 (65) | 121 (101) | 104 (73) | 98 (52) | 95 (50) | 0.18 |
FFM (kg), mean (SD) | | | | | | <0.001 |
Male, mean (SD) | 58.5 (6.9) | 59.5 (7.4) | 56.4 (5.7) | | | |
Female, mean (SD) | 41.9 (5.3) | | | 42.4 (4.8) | 41.3 (5.9) | |
FFMI (kg/m2), median (IQR) | | | | | | <0.001 |
Male, median (IQR) | 19.4 (2.2) | 19.5 (2.4) | 19.3 (2.3) | | | |
Female, median (IQR) | 16.7 (1.5) | | | 16.7 (2.3) | 16.7 (2.8) | |
FMI (kg/m2), median (IQR) | | | | | | <0.001 |
Male, median (IQR) | 7.3 (3.0) | 7.8 (3.2) | 7.0 (3.1) | | | |
Female, median (IQR) | 10.1 (3.6) | | | 10.1 (3.0) | 9.9 (4.6) | |
FM%, mean (SD) | | | | | | <0.001 |
Male, mean (SD) | 27.2 (5.3) | 28.0 (5.4) | 26.3 (5.2) | | | |
Female, mean (SD) | 38.0 (6.3) | | | 37.7 (6.6) | 38.4 (6.1) | |
Plasma total cholesterol, (mmol/l), mean (SD) | 4.9 (1.0) | 4.7 (0.94) | 4.6 (0.93) | 5.4 (1.3) | 5.2 (0.93) | 0.007 |
Plasma LDL cholesterol, (mmol/l), mean (SD) | 2.5 (0.75) | 2.5 (0.78) | 2.3 (0.65) | 2.6 (0.88) | 2.6 (0.69) | 0.18 |
Plasma HDL cholesterol, (mmol/l), mean (SD) | 1.4 (0.33) | 1.2 (0.25) | 1.3 (0.38) | 1.5 (0.50) | 1.5 (0.29) | <0.001 |
Plasma albumin (g/l), mean (SD) | 38.1 (2.7) | 38.6 (2.7) | 37.4 (2.5) | 38.4 (3.0) | 37.2 (2.4) | 0.39 |
Serum IGF-I*, μg/l, mean (SD) | 131.1 (46.6) | 131.5 (44.9) | 134.0 (44.0) | 131.8 (56.3) | 120.6 (44.7) | 0.52 |
Plasma CRP, mg/l, median (IQR) | 1.9 (2.7) | 1.9 (2.3) | 2.6 (2.3) | 1.4 (3.7) | 2.3 (2.9) | 0.55 |
All participants were able to walk outside according to the mobility item of the MNA-SF questionnaire. A reduced SPPB (≤8 p) was observed in 28 %, with the highest occurrence in old women (Table
2). A low gait speed (<1 m/s) was observed in 28 %, with the highest occurrence in older women (Table
2). FMIs above the 90
th percentile of a Swiss reference population [
27] were observed in 26 %, and 87 % of the individuals had FM% values above the reference value. FFMI was low (defined as < 25
th percentile of a Swiss reference population) in 14 % of the individuals [
27]. Sarcopenia, i.e., the combined finding of reduced FFMI with either low SPPB (≤8 points) or low gait speed (<1.0 m/s), was observed in 7 %. None of these sarcopenic individuals were also obese; thus, SO was not observed [
9,
29].
The levels of physical activity (PASE) ranged from 0–312 points, with no significant difference between men and women. Motor function was generally high; 67 % of the individuals reached the maximum of 55 points in the M-MAS UAS-99 (range 39–55). This indicates that the stroke population in this study only had minor to moderate impairments and activity restrictions.
Next, we analysed potential denominators of mobility (SPPB). The co-variates were selected from measures of body composition, nutritional status, and physical activity (PASE and M-MAS). For the correlation and regression analyses between SPPB and MNA-SF, the “mobility” item was removed from the MNA-SF to avoid multicollinearity. For this analysis MNA-SF 11–12 points indicated normal nutritional status, whereas scores of ≤ 10 indicated risk for malnutrition, and this cut-off was used to dichotomise nutritional status. Considering all individuals, univariate analysis revealed significant associations between SPPB and age (r = −0.33,
P = 0.044), PASE (r = 0.51,
P < 0.001), nutritional status (MNA-SF without the “mobility” item) (r = 0.33,
P < 0.001), and gender (r = 0.17,
P = 0.054). Gender-separated associations are presented in Table
3. There were no univariate associations between SPPB and any body composition measure including FFMI in either the whole group or when separated by gender. The M-MAS showed a ceiling effect and was therefore not used in the multivariate regression analyses.
Table 3
Univariate associations between mobility (SPPB) and age, body composition, physical activity level and nutritional status, 1–3 years after stroke
Age, years | −0.29 | 0.065 | −0.31 | 0.003 |
FFMI, (kg/m2) | 0.015 | 0.89 | −0.033 | 0.83 |
FMI, (kg/m2) | −0.012 | 0.94 | −0.046 | 0.66 |
PASE (points, ≥0) | 0.45 | 0.003 | 0.5 | <0.001 |
MNA-SF | 0.32 | 0.039 | 0.31 | 0.003 |
We used the cut-off of ≤ 8 points to dichotomise mobility into high and low mobility [
6] for logistic regression analyses. All estimates were adjusted for age (65–74 and 75–85 years) and gender. When the remaining variables were tested for multi-collinearity by cross-tabulation, the PASE scores (divided into tertiles indicating low, medium, and high physical activity), nutritional status, age (10-year intervals), and gender were selected as independent variables in the regression analyses with SPPB as the dependent variable. Table
4 shows the result of the univariate and the adjusted multivariate logistic regression analyses, indicating that low mobility was related to the risk of malnutrition (MNA-SF, OR 4.3, CI 1.7–10.5), low physical activity (PASE) (OR 6.5, CI 2.0–21.2), medium physical activity (PASE) (OR 3.5, CI 1.3–9.6) and, finally, every 10 years of increased age (OR 0.36, CI 0.15–0.85).
Table 4
Logistic regression with low mobility (SPPB) as dependent variable in 134 cases, 1–3 years after stroke
Explanatory variables | | | | | | |
PASE medium level | 3.3 | 1.3 to 8.1 | 0.012 | 3.5 | 1.3 to 9.6 | 0.013 |
PASE low level | 7.7 | 2.6 to 22.9 | <0.001 | 6.5 | 2.0 to 21.2 | 0.02 |
MNA-SF (except mobility)a
| 4.3 | 1.9 to 9.8 | <0.001 | 4.3 | 1.7 to 10.5 | 0.02 |
Gender | 1.3 | 0.58 to 2.99 | 0.48 | 1.13 | 0.83 to 0.98 | 0.79 |
Age per 10 years | 0.38 | 0.18 to 0.81 | 0.013 | 0.36 | 0.15 to 0.85 | 0.02 |
Interestingly, when the individual components of SPPB were tested for potential univariate associations, time for five chair-stands (s) revealed significant associations with physical activity (r = −0.35, P > 0.001), nutritional status (r = −0.22, P = 0.012), and FMI (r = 0.21, P = 0.017).
Discussion
This study on ambulatory community-dwelling individuals one to 3 years after stroke displayed some confirmative and some novel findings. Not surprisingly, more than one in five individuals were obese. Reduced mobility (SPPB) and low gait speed in 29 % and 28 %, respectively, was also expected. The prevalence of sarcopenia was approximately 7 % according to the used definition. None of the individuals had SO. Fourteen percent of the individuals were identified as at risk for malnutrition, whereas none were classified as malnourished. The risk of malnutrition according to the MNA-SF, old age, and reduced levels of self-reported physical activity (PASE) were associated with an exponential risk for low mobility (SPPB). A somewhat unexpected result was that body composition measures (e.g., FMI and FFMI) were not related to SPPB scores. Therefore, the hypothesis that reduced FFMI was associated with reduced mobility could not be confirmed. However, the other hypotheses concerning the associations of the SPPB with nutritional status and self-reported physical activity were confirmed.
The prevalence of sarcopenia was unexpectedly low (7 %) in this cohort of post-stroke subjects and is generally in line with findings in community-dwelling older individuals [
6]. The observed low prevalence is mainly related to the apparently well-preserved muscle mass of the subjects, as they appeared to have an even greater muscle mass than the Swiss healthy reference population. This finding is difficult to explain, but it may relate to the fact that the weight was higher in the post-stroke cohort and that obesity was common, which is known to be related to higher muscle mass [
31,
32]. It is also important to realise that most of the included individuals in this study had suffered a minor stroke without a pronounced hemiparesis and with preserved walking capacity. In Sweden, 74 % of stroke patients are released to their home after acute stroke. This fact indicates that the current study is fairly representative of community-dwelling post-stroke individuals. There is a stroke-specific type of sarcopenia [
31,
32] that primarily occurs in patients with more severe disease than observed among these study participants. To our knowledge, this is the first report on the prevalence of sarcopenia in community-dwelling individuals after stroke.
The patients’ diet histories were not recorded; thus, it is difficult to establish whether a high energy intake or physical inactivity was the major cause for obesity. Despite inconsistent findings, whole-body FM appears to increase between 6 and 12 months post-stroke, whereas no change in FFM has been reported over time [
33,
34]. Interestingly, recent studies have reported lower mortality, improved functional outcomes, and a lower risk for re-admission from recurrent stroke in obese compared with lean stroke patients [
31,
35]. This is sometimes referred to as the obesity paradox [
35].
The prevalence of malnutrition or being at risk for malnutrition (14 %) according to MNA-SF in the present study was lower than the corresponding 37 % reported from a European compilation of community-living older adults (age 79 years) without stroke [
36]. Although the mean age was 5 years lower in the current study group of post-stroke community-living individuals, the combined findings indicate that the study group was in fairly good condition.
As illustrated by the M-MAS UAS-99 results, motor function was high. If more disabled individuals had been included, the prevalence rates of sarcopenia and SO would likely have been higher. The observation of overweight and obesity not being associated with reduced mobility was interesting and somewhat unexpected and contrasted with earlier findings [
9]. As already indicated, it was also unexpected that alterations in FFMI were not related to mobility as measured by the SPPB. This result suggests that muscle mass is not always crucial for function, which has also been observed in other studies performed in elderly populations [
32,
37]. Perhaps this lack of relationship between muscle mass and function is even more pronounced in stroke survivors for whom neurological damage also contributes to strength and function.
The reduced PASE scores recorded in the current study are in agreement with previous reports of community-living individuals with stroke, corresponding to 67 % of gender- and age-matched control values [
38]. It is unlikely that the observed reduced mobility and physical activity were primarily related to neurological damage due to the previous stroke because only a few individuals had motor impairments.
The current study has limitations that need to be acknowledged. About half of the eligible population could not be examined, which may limit the generalisability of the results. Individuals with more severe disabilities (e.g., unable to stand safely) could not perform the BIA procedure, which affects the generalisation of the results to more disabled stroke patients, e.g., nursing-home residents. Individuals in the Swiss reference population conducted BIA in the supine position. In the current study BIA was performed in standing position, which may differ from BIA measurement performed in lying. Furthermore, individuals with subarachnoid haemorrhage were not included. All individuals in this study were community-dwelling, indicating better functional and nutritional status compared with nursing home residents. According to the International Classification of Functioning Disability and Health (ICF), disability is an umbrella term for impairments, activity limitations, and participation restrictions [
39]. The measures of this study covered a great part of the ICF description of disability by including the motor function (M-MAS UAS-99), mobility (SPPB), and gait speed (10 mWT). Activity limitations and to some extent also participation restrictions were covered by the PASE, measuring exercise, leisure-time activities and voluntary work. Moreover, the cross-sectional design of the study limits the possibility to make causal inferences. Further studies on body composition and sarcopenia in stroke populations with minor to moderate stroke are needed [
34].
Conclusions
We conclude that in community-living subjects assessed one to 3 years after stroke, reduced mobility according to SPPB was related to risks of malnutrition (according to the MNA-SF), low and medium physical activity (according to PASE) but not to alterations in body composition, e.g., FFMI and FMI. Obesity, sarcopenia, and risk of malnutrition were observed in about one-third of the study population. These results suggest that stroke rehabilitation efforts could benefit from promoting a healthy and nutritious diet and physical activity to optimise mobility, reduce obesity, and avoid sarcopenia. Intervention studies are needed to address the potential benefits of such lifestyle changes.
Competing interests
None of the authors have any conflicts of interest to disclose.
Authors’ contributions
BV wrote the manuscript. BV, TC, BL, KH, and LZ were involved in the conception and design, reviewed and edited the manuscript, and contributed with discussions. BV was involved in the acquisition, analysis, and interpretation of data. All authors read and approved the final manuscript.