Journal of Aging and Physical Activity, 2016, 24, 92 -100 http://dx.doi.org/10.1123/japa.2014-0202 © 2016 Human Kinetics, Inc.
ORIGINAL RESEARCH
Physical Fitness in Older People with Mild Cognitive Impairment and Dementia Karin Hesseberg, Hege Bentzen, Anette Hylen Ranhoff, Knut Engedal, and Astrid Bergland Maintenance of physical activity and good physical fitness is important for functional independence. This study had two aims: examine the physical fitness level in older persons with mild cognitive impairment (MCI) or dementia, and examine the relationship between the components of physical fitness and cognitive domains in this group. The cross-sectional study included community-living older people ≥ 65 years of age with MCI or dementia. Physical fitness and cognition were assessed using the Senior Fitness Test and five cognitive tests. Most of the participants scored below the criteria for maintaining physical independence in later years. There were significant associations between the components of physical fitness and cognition, except flexibility. Declines in executive function were most related to declines in physical fitness. These factors should receive more attention in people with MCI and dementia because they risk losing independence. Keywords: physical fitness, physical activity, mild cognitive impairment, dementia, aging
Dementia is a major cause of disability and dependency among older people, and the need for care for older people with dementia is anticipated to increase because the number of older people is increasing (World Health Organization, 2010a; World Health Organization & Alzheimer’s Disease International, 2012). Dementia is an umbrella term for brain disorders that describes a variety of diseases and conditions, usually of a chronic or progressive nature, that develop when certain brain cells are damaged and cerebral brain atrophy occurs (Thies & Bleiler, 2013). Mild cognitive impairment (MCI) describes the possible transitional state between normal aging and dementia (DeCarli, 2003). MCI is assumed to be a high-risk condition for the development of dementia, even though only approximately 50% of those with a diagnosis of MCI will develop dementia (Alzheimer’s Association 2009; Gauthier et al., 2006; Thies & Bleiler, 2013). Because we still have no curative treatment for dementia, more research is needed to assess other potential amenable factors than medication that could be beneficial for the prevention of dementia and to increase the possibility for independent living (Rolland, Abellan van Kan, & Vellas, 2010). In this study, components of physical fitness, such as muscle strength, aerobic endurance, flexibility, body composition, dynamic balance, and agility, were assessed by using the Senior Fitness Test (SFT) (Rikli & Jones, 2012), which facilitates a focus on nonpharmacological interventions. The concept of physical fitness is related to the capacity to perform activities of daily living (ADL) (Rikli & Jones, 2012). The capacity to perform ADL is a defining diagnostic feature of MCI and dementia as well, and we find it important to focus on the ability for independent living in this patient group (Winblad et al., 2004; World Health Organization, 2010b). Good physical fitness can contribute to maintenance of independent living Hesseberg, Bentzen, and Bergland are with Oslo and Akershus University College of Applied Sciences, Norway. Hesseberg is also with Diakonhjemmet Hospital, Norway. Hylen Ranhoff is with Diakonhjemmet Hospital, Norway; Kavli Research Centre for Geriatrics and Dementia, Haraldsplass Hospital, Bergen, Norway; and the Department of Clinical Science, University of Bergen, Norway. Engedal is with the Norwegian Centre for Aging and Health, Vestfold Hospital Trust, Tønsberg, Norway. Address author correspondence to Karin Hesseberg at [email protected]. 92
in older people with MCI and dementia (Blankevoort et al., 2010; Paterson, Jones, & Rice, 2007; Taylor, 2014). However, the scores of the physical fitness components included in the SFT of persons newly diagnosed with MCI and dementia are not yet described in the literature. Physical fitness relates to the ability to perform physical activity because higher amounts of physical activity lead to improved physical fitness and vice versa (Caspersen, Powell, & Christenson, 1985). Physical fitness is a set of attributes that people have—or can—achieve, and physical activity is related to the movements that people perform (Caspersen et al., 1985). Low levels of physical activity and poor physical fitness are common in older people, although people over 65 years of age are recommended to perform higher levels of physical activity, in order to maintain health and physical independence, than the minimum recommendation of physical activity for adults (Nelson et al., 2007). The minimum recommendations for adults include moderate intensity aerobic physical activity for a minimum of 30 min on five days each week or vigorous intensity aerobic activity for a minimum of 20 min on three days each week (Haskell et al., 2007). The recommendations for older people include several additions, including: that the recommended intensity of aerobic activity takes into account the older adult’s aerobic fitness; activities that maintain or increase flexibility are recommended; and balance exercises are recommended for older adults at risk for fall, in addition to muscle-strengthening activity, reducing sedentary behavior, and risk management (Nelson et al., 2007). Physical activity interventions to improve components of physical fitness provide health benefits, including promising effects on cognitive function and the postponement or prevention of MCI and dementia in older people without known cognitive impairment. Furthermore, physical activity has a positive impact on cognitive decline in those at early stages of cognitive impairment and can slow down the decline in physical fitness and the deterioration in the capacity to perform ADL in older people with dementia (Angevaren, 2008; Barnes, Yaffe, Satariano, & Tager, 2003; Blankevoort et al., 2010; Colcombe & Kramer, 2003; Forbes, Thiessen, Blake, Forbes, & Forbes, 2013; Kirk-Sanchez & McGough, 2014; Lee et al., 2012; Nagamatsu et al., 2013; Nagamatsu, Handy, Hsu, Voss, & Liu-Ambrose, 2012; Nelson et al., 2007; Pitkala, Savikko, Poysti,
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Physical Fitness with MCI and Dementia 93
Strandberg, & Laakkonen, 2013; Polidori, Nelles, & Pientka, 2010; Sofi et al., 2011). ADL include basic activities such as bathing, dressing, and mobility, as well as more complex instrumental ADL (I-ADL), such as climbing stairs, doing housework, running errands, and engaging in personal interests (Lawton & Brody, 1969; Rikli & Jones, 2012). For the successful performance of ADL, cognitive abilities are necessary to achieve specific goals or intentions (Martyr & Clare, 2012; Shumway-Cook & Woollacott, 2012; Strauss, Sherman, & Spreen, 2006). Cognitive function is similar to physical fitness in that it comprises several interrelated domains such as memory, attention, visual–spatial abilities, and executive function (EF) (Strauss et al., 2006). Associations exist between different domains of cognitive function and components of physical fitness related to independent living, but studies on these associations in older people with MCI and dementia remain scarce. Studies report associations between cognitive function and gait speed and mobility (Auyeung et al., 2008; Donoghue et al., 2012; McGough et al., 2011; Persad, Jones, Ashton-Miller, Alexander, & Giordani, 2008; Takata et al., 2008), muscle strength (Auyeung et al., 2008; Takata et al., 2008), and balance and falling risk (Hsu, Nagamatsu, Davis, & Liu-Ambrose, 2012; Takata et al., 2008; Tangen, Engedal, Bergland, Moger, & Mengshoel, 2014). There are hardly any studies reporting associations between flexibility and cognitive function (Park & Bae, 2012), and there is no agreement in the literature regarding the relationship between body mass index (BMI) and MCI and dementia (Anstey, Cherbuin, Budge, & Young, 2011; Cronk, Johnson, Burns, & Alzheimer’s Disease Neuroimaging Initiative, 2010; Doruk, Naharci, Bozoglu, Isik, & Kilic, 2010). Physical fitness contains multiple components, such as those included in the SFT. More information about which components of physical fitness are most reduced and which components are related to cognitive function in older people with MCI and dementia might be explored when we use this test. This information may help to direct interventions to the affected components of physical fitness to initiate individually-tailored training programs. In addition, effective prevention and rehabilitation strategies to maintain functional independency and avoid institutionalization could be established (Blankevoort et al., 2010; Luppa et al., 2010). Furthermore, information about the relationships between components of physical fitness and cognition can be useful to initiate randomized controlled studies (RCT). Two aims were addressed in this study: (1) to explore the performance level of the various components of physical fitness in older persons with MCI or dementia; and (2) to examine the relationship between the components of physical fitness and cognitive domains in older people with MCI or dementia.
Methods
the inclusion and exclusion criteria were asked to participate in the study. Participants were gathered from: patients visiting one of the clinics between January 2011 and January 2014 (76 participants); patients visiting one of the clinics between May 2011 and May 2013 (12 participants); patients visiting one of the clinics between June 2011 and October 2011 (4 participants); and patients visiting one clinic between April 2013 and November 2013 (6 participants). In all, there were 98 participants.
Diagnostic Procedures Physicians at the memory clinics diagnosed the patients as either having MCI, dementia, or no impairment. The ICD-10 classification for research was used when diagnosing dementia and subtypes of dementia, and the Winblad criteria were used when diagnosing MCI (Winblad et al., 2004). The Winblad criteria include: not normal, not demented (does not meet criteria [DSMI-5, ICD-10] for dementia syndrome); cognitive decline, which is self- and/or informant-reported with impairment on objective cognitive tasks, and/or evidence of decline over time on objective cognitive tasks; and preserved basic activities of daily living/minimal impairment in complex instrumental functions (Winblad et al., 2004). Subtypes of MCI such as amnestic and nonamnestic MCI have been proposed (Gauthier et al., 2006), but in this study such subgroups were not made according to lack of information available. Diagnoses were based on a standard comprehensive examination protocol and included taking a medical history and information from a family caregiver, testing cognitive function, a physical examination, and a psychiatric evaluation with a primary emphasis on depression (Braekhus, Ulstein, Wyller, & Engedal, 2011). Cognitive tests included the Mini-Mental State Examination (MMSE), the clock drawing test (CDT), the Trail Making Tests A and B (TMTA and TMTB), the 10-word-list learning test and copying figures from the Consortium to establish a registry for Alzheimer’s disease (CERAD), and the Controlled Oral Word Association (COWA) (Braekhus et al., 2011). Structural brain examinations were performed with magnetic resonance imaging (MRI) or computed tomography (CT) on all patients. Functional examinations using single photon emission computed tomography (SPECT) and spinal fluid examinations (biomarkers) were performed on patients where the clinicians needed more information to make a correct diagnosis (Braekhus et al., 2011).
Demographic and Clinical Information Information on demographic characteristics, including age, sex, education, and marital status, and information about depression, the diagnosis, and the cognitive assessments were retrieved from the NDR.
Cognitive Assessments
Design and Participants The study had a cross-sectional design and is part of an ongoing longitudinal study with a one-year follow-up. Community-living older people ≥ 65 years of age with MCI or dementia were included. The participants were recruited from four memory clinics in Norway after an initial examination to confirm or exclude MCI and dementia. Diagnostic procedures for MCI and dementia are described in the section below. Exclusion criteria were reported terminal disease with an expected lifespan of less than one year due to the longitudinal study design. All patients who agreed to be included in the Norwegian Dementia Registry (NDR) and fulfilled
Five cognitive tests that covered various cognitive domains were included in this study: global cognition, visual–spatial abilities, EF, attention, processing speed, visual and verbal working memory, planning, and ability to go back and forth between multiple tasks (set-shift). The MMSE was used to assess global cognition and has a score range of 0–30, where a higher score indicates better performance (Folstein, Folstein, & McHugh, 1975). The CDT evaluates many cognitive skills including visual–spatial abilities and EF, and a 6-point score from 0–5 was used (Shulman, 2000; Strauss et al., 2006). Test scores of 4–5 indicate a normal score according to the scoring procedure of Shulman (2000). The TMTA and TMTB
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94 Hesseberg et al.
were used to test attention and processing speed, and to test EF and set-shift, respectively (Reitan & Wolfson, 1993). The tests are timed in seconds and categorized into four categories based on normative age-adjusted time intervals. The 10-word-list learning test from the CERAD was used to evaluate the learning aspect of memory, where a list of 10 words was presented three times, and the participants were asked to recall the words. Scoring of 0–30 was used to measure the total number of correct words learned (10-word recall) and scores of 0–10 were used to measure the correct words recalled after 5 min of distraction (10-word delayed) (Welsh et al., 1994). Experienced nurses, occupational therapists, and physicians at the memory clinics conducted testing.
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Assessment of Physical Fitness The SFT is a widely-used standardized and safe assessment for providing information about components of physical fitness in older people (Rikli & Jones, 2012). The SFT is a reliable test battery for assessing physical fitness in older people ≥ 60 years (ICC values 0.80–0.98) (Rikli & Jones, 2012), including those with MCI or early dementia (ICC values 0.93–0.98) (Hesseberg, Bentzen, & Bergland, 2015). According to those who developed the SFT, the test does not create a sum score for physical fitness level, but was designed to assess underlying physical components associated with functional mobility such as muscle strength, aerobic endurance, flexibility, body composition, dynamic balance, and agility (Rikli & Jones, 2012). The item scores create a profile of these fitness components associated with independent functioning (Rikli & Jones, 2012). Normative data based on age and sex for over 7,000 adults aged from 60 to 94 years from a population in the United States have been provided (Rikli & Jones, 2012). Scores between the 25th and 75th percentiles in each age and sex group (the middle 50% of the values) are defined as normal. Criterion-referenced fitness standards for maintaining physical independence in later years have also been developed for the SFT (Rikli & Jones, 2012). The cut-off scores for each age and sex group appear to be reasonable estimates of the level of fitness associated with remaining physically mobile and independent in later life (Rikli & Jones, 2012). Criterion standards have not been proposed for the two flexibility items, as there is insufficient evidence documenting the relationship between measures of flexibility and improved functional ability (Rikli & Jones, 2012). The SFT assessments were made in the following order: chair stand test for lower body muscle strength (number of repetitions within 30 s); arm curl test for upper body muscle strength (number of repetitions within 30 s); chair sit-and-reach test for lower body flexibility (distance between fingers and toes); back scratch test for upper body flexibility (distance between the third finger of each hand); 2.45-m up-and-go test (up-and-go) for agility and dynamic balance (time to rise, walk 2.45 m and return to the chair); and 6-min walk test to measure aerobic endurance (distance walked in 6 min). Height and weight were measured to calculate the BMI in kg/m2. More detailed descriptions are presented in the SFT manual (Rikli & Jones, 2012). SFT was assessed by an experienced physiotherapist (KH), and testing was conducted in rooms with adequate space and lighting in the hospitals where the subjects were recruited to ensure optimal performance.
Statistical Analysis Data are presented as the mean and standard deviation (SD) for continuous variables and as percentages for categorical variables. Differences between the groups, MCI and dementia, were tested
by the chi-square test and Fisher’s exact test for categorical data, and by independent sample t test for continuous data. Descriptive statistics with proportions were used to examine physical fitness scores for the study population compared with normative scores and with criteria used for measuring physical independence. Associations between physical fitness and cognitive performance were analyzed in a multiple linear regression analysis with the physical fitness parameters as dependent variables. Independent variables included the cognitive tests, MMSE, CDT, TMTA, TMTB, and the 10-word-list learning test, as well as the demographic factors of age, sex, education, and marital status. Statistically significant variables in the univariate analysis were included in a subsequent multivariate analysis. Backward removal analyses were used to analyze which cognitive domains (tests) were most related to the components of physical fitness. Bivariate correlations and analysis of multicollinearity were checked to detect any high level of association between independent variables and covariates. Residual plots were inspected, and if the model assumptions were violated, a sensitivity analysis was performed to test the robustness of the results. We considered p < .05 statistically significant. Statistical analyses were performed in SPSS for Windows version 20.0 (IBM Corp., Armonk, NY).
Ethics The study was approved by the Regional Committee for Medical Research Ethics in South-Eastern Norway. The participants were given oral and written information about the study and signed a written informed consent form before taking part. A physician at the memory clinic assessed whether the participants were able to give their consent before they were included in the study. The physicians considered the patient’s evidencing a choice, understanding, appreciation, and reasoning when they assessed the patient’s ability to participate. Our population consisted of older people with MCI and early dementia; at these stages of disease, consent is less problematic in comparison with more severe dementia. To prevent possible injuries or adverse events, the participants were followed closely during the assessments. They were asked if they needed breaks, and they were also instructed that they had the ability to withdraw from further testing and from the entire study at any time. No adverse events were recorded.
Results Of the 98 subjects, there were 45 men and 53 women; 60 were diagnosed with MCI and 38 with dementia. The participants with dementia (40% of the total sample) included Alzheimer’s disease (28%), vascular dementia (1%), and “other dementia” (e.g., dementia due to Parkinson’s disease, Lewy body disease, and frontal lobe dementia) (11%). The MCI diagnosis was not divided into subgroups. The mean age was 78.8 years, mean years of education was 13.5, and 40% were living alone (Table 1). In Table 1 more details regarding demographic characteristics are presented, as well as the scores for the components of the SFT and cognitive assessments of the study population. The demographic characteristics and scores on the SFT revealed no significant differences between MCI and dementia patients with the exception of years of education (p = .05). The MCI group had significantly better scores on four of the five cognitive tests compared with the dementia group. The performance level of the components of physical fitness (SFT) in our study group are compared with the normative data in the SFT and presented in Table 2. Our results show that the proportion of scores over normal was less than 25% in all of the parameters of
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Physical Fitness with MCI and Dementia 95
Table 1 Characteristics of the Participants All M (SD)
MCI %
M (SD)
Dementia
Variable
N
%
M (SD)
%
P-valuea
Gender (% women)
98
54
Diagnosis, MCI or dementia (% MCI)
98
61
52
58
.547
Living alone (% yes)
98
CSDD (% no symptoms, sum score < 6)
59
40
37
45
.426
48
53
40
.325
Age (years)
98
78.8 (7.4)
77.9 (7.2)
80.1 (7.6)
.151
Education (years)
82
13.5 (3.3)
14.0 (3.3)
12.6 (3.1)
.052*
MMSE (score 0–30)
98
24.1 (3.9)
25.5 (2.9)
21.8 (4.3)
< .001**
10-word recall (score 0–30)
95
12.3 (4.5)
13.4 (4.3)
10.6 (4.4)
.003**
10-word delayed (score 0–10)
94
1.9 (2.1)
2.2 (2.0)
1.4 (2.2)
.059
CDT (% normal, score 4–5)
98
51
60
37
.025*
98
3
0
8
.017*
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Cognitive assessment
TMTA, categorized (%) Unable to complete Score lower than –2 SD
36
32
42
Time between –1 and –2 SD
35
33
37
Time better than –1 SD
27
35
13
TMTB, categorized (%) Unable to complete
53
40
73
Score lower than –2 SD
97
13
13
14
Time between –1 and –2 SD
12
18
3
Time better than –1 SD
22
28
11
.005**
Senior fitness test Chair stand (# in 30 s)
98
9.4 (4.3)
9.3 (3.8)
9.6 (4.9)
.724
Arm curl (# in 30 s)
97
13.1 (3.8)
13.0 (4.0)
13.2 (3.6)
.779
Chair sit-and-reach (cm from fingers to toes)
97
–12.0 (12.6)
–11.8 (11.8)
–12.4 (13.8)
.822
Back scratch (cm between the third finger of each hand)
97
–16.4 (12.2)
–16.0 (12.8)
–17.1 (11.4)
.678
2.45 m up-and-go (s)
97
9.0 (3.7)
8.8 (4.1)
9.2 (3.1)
.580
6-min walk (meters)
90
420 (123)
434 (126)
399 ((117)
.196
97
23.8 (3.9)
23.8 (4.3)
23.9 (3.3)
.871
BMI
(kg/m2)
Abbreviations: MCI = mild cognitive impairment; CSDD = Cornell Scale for Depression in Dementia; MMSE = Mini-Mental State Examination; CDT = clock drawing test; TMTA = Trail Making Test A; TMTB = Trail Making Test B; BMI = body mass index. Significant differences between the patient groups (MCI and dementia) analyzed with Chi-square test, Fisher’s exact test, and independent-sample t test. *p < .05; **p < .01. a
the SFT, and that more than 25% of the participants had lower than normal scores in all of the parameters of the SFT with the exception of the arm curl test (Table 2). Table 3 presents the proportion of our study group having scores above and below the cut-off scores for the criteria for maintaining physical independence in later years. The four fitness items assessed showed that 68–85% of the participants had scores below the cut-off for predicting the ability to function independently in later years (Table 3). The results of multiple linear regression analyses regarding the associations between the components of physical fitness and cognitive domains in older people with MCI or dementia are presented in Table 4. The CDT was the only cognitive test significantly associated with lower and upper body muscle strength, represented by the chair stand test and the arm curl test. The associations remained statistically significant after adjusting for covariates (B = 1.75, p = .037
and B = 2.36, p = .002, respectively). The score on CDT was also significantly associated with the BMI after adjusting for covariates: a normal score on the CDT indicated a higher BMI (B = 2.07, p = .009). TMTB and CDT were significantly associated with dynamic balance and agility represented by the up-and-go test in univariate analysis, but TMTB was the only test that remained significant in the multivariate analysis (B = –0.64, p = .026). By inspecting the residual plots, we observed that the model assumptions were violated with the up-and-go test as the dependent variable. A sensitivity analysis was performed, with the same results. The 6-min walk test—representing aerobic endurance—showed a significant association with the TMTB, CDT, and 10-word-list recall in univariate analysis, but TMTB was the only test that remained significant in the multivariate analysis (B = 19.7, p < .001). Participants with better performance on the TMTB (shorter time to do the test) used
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96 Hesseberg et al.
Table 2 Senior Fitness Test Scores Compared with Normative Scores from a Population in the United States Above Normal Scores (%)
Normal Scoresa (%)
Below Normal Scores (%)
Chair stand (# in 30 s)
4
50
46
Arm curl (# in 30 s)
8
67
18
Chair sit-and-reach (cm from fingers to toes)
2
40
56
Back scratch (cm between the third finger of each hand)
11
45
43
2.45 m up-and-go (s)
2
43
6-min walk (meters)
7
58
n = 98 Item
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Significant Variables from Univariate Analysis
p-value
95% CI
R2
Age
–0.14
.015*
–0.25 to 0.03
.12
Clock drawing test
1.75
.037*
0.11 to 3.40
Age
–0.12
.018*
–0.22 to –0.02
55
Clock drawing test
2.36
.002**
0.92 to 3.81
36
Trail Making Test B
0.38
.275
–0.31 to 1.07
Age
0.16
.001**
0.07 to 0.26
Trail Making Test B
–0.64
.026*
–1.21 to –0.08
Clock drawing test
–0.92
.273
–2.58 to 0.74
Age
–6.9
< .001**
Trail Making Test B
19.7
.044*
0.52 to 38.41
Clock drawing test
1.07
.970
–55.71 to 57.86
10-word-list recall
2.59
.378
–3.22 to 8.40
Clock drawing test
2.07
.009**
0.53 to 3.61
Age
–0.09
.102
–0.20 to 0.02
Table 3 Senior Fitness Test Scores Above and Below Cut-off Scores for Recommended Fitness Standards for Predicting the Ability to Function Independently in Later Yearsa
a
Multivariate Analysis Ba
a Normal scores are defined as those between the 25th and 75th percentiles in each age and sex group (the middle 50% of the values).
Above Cut-Off Scores (%)
Below Cut-Off Scores (%)
Chair stand (# in 30 s)
23
77
Arm curl (# in 30 s)
32
68
2.45 m up-and-go (s)
15
85
6-min walk (meters)
27
73
n = 98 Item
Table 4 Associations Between Physical Fitness Items and Cognitive Assessments, Adjusted for Demographic Factors in a Multivariate Analysis
Fitness standards according to Rikli and Jones (2012).
less time to perform the up-and-go test (0.64 s less for each category improvement) and walked longer on the 6-min walk test (19.7 m longer for each category improvement). The chair sit-and-reach and back scratch items, both measuring flexibility, showed no significant association with any of the cognitive tests. The cognitive tests MMSE, TMTA, and the 10-word-list recall and delayed test showed no significant association with the components of physical fitness in the univariate analysis. The only exception was a significant association between the 10-word-list recall and the 6-min walk test in univariate analysis, but not in the multivariate analysis.
Discussion In this study we explored the performance level of the components of physical fitness in older persons with MCI or dementia and examined the relationship between the components of physical fitness and different aspects of cognition in community-dwelling older people with MCI or dementia. Overall, the study demonstrated that the older people recently diagnosed with MCI or dementia showed a lower level of physical fitness on all of the physical fitness items except the arm curl test when compared with the normative data of the SFT (Rikli & Jones, 2012). Criteria to predict the ability to function independently in later years were provided for the SFT (Rikli & Jones, 2012), and a high proportion of the participants (68–85%) in this study scored below these cut-off scores. Furthermore, significant associations between physical fitness and cognition were found in
Chair stand test (n = 98)
Arm-curl test (n = 97) .18
Up-and-go (n = 97) .17
6-min walk (n = 86) –10.25 to –3.64 .23
Body mass index (n = 97) .07
Note. Demographic factors in the univariate analysis included age, sex, marital status, and years of education. Sex was included in the multivariate analysis but was not significant in any of the analyses. Cognitive assessments in the univariate analysis: Mini-Mental Status Examination, 10-word-list recall and delayed test, Trail Making Test A, Trail Making Test B, and clock drawing test. a B = unstandardized coefficient. *p
ORIGINAL RESEARCH
Physical Fitness in Older People with Mild Cognitive Impairment and Dementia Karin Hesseberg, Hege Bentzen, Anette Hylen Ranhoff, Knut Engedal, and Astrid Bergland Maintenance of physical activity and good physical fitness is important for functional independence. This study had two aims: examine the physical fitness level in older persons with mild cognitive impairment (MCI) or dementia, and examine the relationship between the components of physical fitness and cognitive domains in this group. The cross-sectional study included community-living older people ≥ 65 years of age with MCI or dementia. Physical fitness and cognition were assessed using the Senior Fitness Test and five cognitive tests. Most of the participants scored below the criteria for maintaining physical independence in later years. There were significant associations between the components of physical fitness and cognition, except flexibility. Declines in executive function were most related to declines in physical fitness. These factors should receive more attention in people with MCI and dementia because they risk losing independence. Keywords: physical fitness, physical activity, mild cognitive impairment, dementia, aging
Dementia is a major cause of disability and dependency among older people, and the need for care for older people with dementia is anticipated to increase because the number of older people is increasing (World Health Organization, 2010a; World Health Organization & Alzheimer’s Disease International, 2012). Dementia is an umbrella term for brain disorders that describes a variety of diseases and conditions, usually of a chronic or progressive nature, that develop when certain brain cells are damaged and cerebral brain atrophy occurs (Thies & Bleiler, 2013). Mild cognitive impairment (MCI) describes the possible transitional state between normal aging and dementia (DeCarli, 2003). MCI is assumed to be a high-risk condition for the development of dementia, even though only approximately 50% of those with a diagnosis of MCI will develop dementia (Alzheimer’s Association 2009; Gauthier et al., 2006; Thies & Bleiler, 2013). Because we still have no curative treatment for dementia, more research is needed to assess other potential amenable factors than medication that could be beneficial for the prevention of dementia and to increase the possibility for independent living (Rolland, Abellan van Kan, & Vellas, 2010). In this study, components of physical fitness, such as muscle strength, aerobic endurance, flexibility, body composition, dynamic balance, and agility, were assessed by using the Senior Fitness Test (SFT) (Rikli & Jones, 2012), which facilitates a focus on nonpharmacological interventions. The concept of physical fitness is related to the capacity to perform activities of daily living (ADL) (Rikli & Jones, 2012). The capacity to perform ADL is a defining diagnostic feature of MCI and dementia as well, and we find it important to focus on the ability for independent living in this patient group (Winblad et al., 2004; World Health Organization, 2010b). Good physical fitness can contribute to maintenance of independent living Hesseberg, Bentzen, and Bergland are with Oslo and Akershus University College of Applied Sciences, Norway. Hesseberg is also with Diakonhjemmet Hospital, Norway. Hylen Ranhoff is with Diakonhjemmet Hospital, Norway; Kavli Research Centre for Geriatrics and Dementia, Haraldsplass Hospital, Bergen, Norway; and the Department of Clinical Science, University of Bergen, Norway. Engedal is with the Norwegian Centre for Aging and Health, Vestfold Hospital Trust, Tønsberg, Norway. Address author correspondence to Karin Hesseberg at [email protected]. 92
in older people with MCI and dementia (Blankevoort et al., 2010; Paterson, Jones, & Rice, 2007; Taylor, 2014). However, the scores of the physical fitness components included in the SFT of persons newly diagnosed with MCI and dementia are not yet described in the literature. Physical fitness relates to the ability to perform physical activity because higher amounts of physical activity lead to improved physical fitness and vice versa (Caspersen, Powell, & Christenson, 1985). Physical fitness is a set of attributes that people have—or can—achieve, and physical activity is related to the movements that people perform (Caspersen et al., 1985). Low levels of physical activity and poor physical fitness are common in older people, although people over 65 years of age are recommended to perform higher levels of physical activity, in order to maintain health and physical independence, than the minimum recommendation of physical activity for adults (Nelson et al., 2007). The minimum recommendations for adults include moderate intensity aerobic physical activity for a minimum of 30 min on five days each week or vigorous intensity aerobic activity for a minimum of 20 min on three days each week (Haskell et al., 2007). The recommendations for older people include several additions, including: that the recommended intensity of aerobic activity takes into account the older adult’s aerobic fitness; activities that maintain or increase flexibility are recommended; and balance exercises are recommended for older adults at risk for fall, in addition to muscle-strengthening activity, reducing sedentary behavior, and risk management (Nelson et al., 2007). Physical activity interventions to improve components of physical fitness provide health benefits, including promising effects on cognitive function and the postponement or prevention of MCI and dementia in older people without known cognitive impairment. Furthermore, physical activity has a positive impact on cognitive decline in those at early stages of cognitive impairment and can slow down the decline in physical fitness and the deterioration in the capacity to perform ADL in older people with dementia (Angevaren, 2008; Barnes, Yaffe, Satariano, & Tager, 2003; Blankevoort et al., 2010; Colcombe & Kramer, 2003; Forbes, Thiessen, Blake, Forbes, & Forbes, 2013; Kirk-Sanchez & McGough, 2014; Lee et al., 2012; Nagamatsu et al., 2013; Nagamatsu, Handy, Hsu, Voss, & Liu-Ambrose, 2012; Nelson et al., 2007; Pitkala, Savikko, Poysti,
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Physical Fitness with MCI and Dementia 93
Strandberg, & Laakkonen, 2013; Polidori, Nelles, & Pientka, 2010; Sofi et al., 2011). ADL include basic activities such as bathing, dressing, and mobility, as well as more complex instrumental ADL (I-ADL), such as climbing stairs, doing housework, running errands, and engaging in personal interests (Lawton & Brody, 1969; Rikli & Jones, 2012). For the successful performance of ADL, cognitive abilities are necessary to achieve specific goals or intentions (Martyr & Clare, 2012; Shumway-Cook & Woollacott, 2012; Strauss, Sherman, & Spreen, 2006). Cognitive function is similar to physical fitness in that it comprises several interrelated domains such as memory, attention, visual–spatial abilities, and executive function (EF) (Strauss et al., 2006). Associations exist between different domains of cognitive function and components of physical fitness related to independent living, but studies on these associations in older people with MCI and dementia remain scarce. Studies report associations between cognitive function and gait speed and mobility (Auyeung et al., 2008; Donoghue et al., 2012; McGough et al., 2011; Persad, Jones, Ashton-Miller, Alexander, & Giordani, 2008; Takata et al., 2008), muscle strength (Auyeung et al., 2008; Takata et al., 2008), and balance and falling risk (Hsu, Nagamatsu, Davis, & Liu-Ambrose, 2012; Takata et al., 2008; Tangen, Engedal, Bergland, Moger, & Mengshoel, 2014). There are hardly any studies reporting associations between flexibility and cognitive function (Park & Bae, 2012), and there is no agreement in the literature regarding the relationship between body mass index (BMI) and MCI and dementia (Anstey, Cherbuin, Budge, & Young, 2011; Cronk, Johnson, Burns, & Alzheimer’s Disease Neuroimaging Initiative, 2010; Doruk, Naharci, Bozoglu, Isik, & Kilic, 2010). Physical fitness contains multiple components, such as those included in the SFT. More information about which components of physical fitness are most reduced and which components are related to cognitive function in older people with MCI and dementia might be explored when we use this test. This information may help to direct interventions to the affected components of physical fitness to initiate individually-tailored training programs. In addition, effective prevention and rehabilitation strategies to maintain functional independency and avoid institutionalization could be established (Blankevoort et al., 2010; Luppa et al., 2010). Furthermore, information about the relationships between components of physical fitness and cognition can be useful to initiate randomized controlled studies (RCT). Two aims were addressed in this study: (1) to explore the performance level of the various components of physical fitness in older persons with MCI or dementia; and (2) to examine the relationship between the components of physical fitness and cognitive domains in older people with MCI or dementia.
Methods
the inclusion and exclusion criteria were asked to participate in the study. Participants were gathered from: patients visiting one of the clinics between January 2011 and January 2014 (76 participants); patients visiting one of the clinics between May 2011 and May 2013 (12 participants); patients visiting one of the clinics between June 2011 and October 2011 (4 participants); and patients visiting one clinic between April 2013 and November 2013 (6 participants). In all, there were 98 participants.
Diagnostic Procedures Physicians at the memory clinics diagnosed the patients as either having MCI, dementia, or no impairment. The ICD-10 classification for research was used when diagnosing dementia and subtypes of dementia, and the Winblad criteria were used when diagnosing MCI (Winblad et al., 2004). The Winblad criteria include: not normal, not demented (does not meet criteria [DSMI-5, ICD-10] for dementia syndrome); cognitive decline, which is self- and/or informant-reported with impairment on objective cognitive tasks, and/or evidence of decline over time on objective cognitive tasks; and preserved basic activities of daily living/minimal impairment in complex instrumental functions (Winblad et al., 2004). Subtypes of MCI such as amnestic and nonamnestic MCI have been proposed (Gauthier et al., 2006), but in this study such subgroups were not made according to lack of information available. Diagnoses were based on a standard comprehensive examination protocol and included taking a medical history and information from a family caregiver, testing cognitive function, a physical examination, and a psychiatric evaluation with a primary emphasis on depression (Braekhus, Ulstein, Wyller, & Engedal, 2011). Cognitive tests included the Mini-Mental State Examination (MMSE), the clock drawing test (CDT), the Trail Making Tests A and B (TMTA and TMTB), the 10-word-list learning test and copying figures from the Consortium to establish a registry for Alzheimer’s disease (CERAD), and the Controlled Oral Word Association (COWA) (Braekhus et al., 2011). Structural brain examinations were performed with magnetic resonance imaging (MRI) or computed tomography (CT) on all patients. Functional examinations using single photon emission computed tomography (SPECT) and spinal fluid examinations (biomarkers) were performed on patients where the clinicians needed more information to make a correct diagnosis (Braekhus et al., 2011).
Demographic and Clinical Information Information on demographic characteristics, including age, sex, education, and marital status, and information about depression, the diagnosis, and the cognitive assessments were retrieved from the NDR.
Cognitive Assessments
Design and Participants The study had a cross-sectional design and is part of an ongoing longitudinal study with a one-year follow-up. Community-living older people ≥ 65 years of age with MCI or dementia were included. The participants were recruited from four memory clinics in Norway after an initial examination to confirm or exclude MCI and dementia. Diagnostic procedures for MCI and dementia are described in the section below. Exclusion criteria were reported terminal disease with an expected lifespan of less than one year due to the longitudinal study design. All patients who agreed to be included in the Norwegian Dementia Registry (NDR) and fulfilled
Five cognitive tests that covered various cognitive domains were included in this study: global cognition, visual–spatial abilities, EF, attention, processing speed, visual and verbal working memory, planning, and ability to go back and forth between multiple tasks (set-shift). The MMSE was used to assess global cognition and has a score range of 0–30, where a higher score indicates better performance (Folstein, Folstein, & McHugh, 1975). The CDT evaluates many cognitive skills including visual–spatial abilities and EF, and a 6-point score from 0–5 was used (Shulman, 2000; Strauss et al., 2006). Test scores of 4–5 indicate a normal score according to the scoring procedure of Shulman (2000). The TMTA and TMTB
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94 Hesseberg et al.
were used to test attention and processing speed, and to test EF and set-shift, respectively (Reitan & Wolfson, 1993). The tests are timed in seconds and categorized into four categories based on normative age-adjusted time intervals. The 10-word-list learning test from the CERAD was used to evaluate the learning aspect of memory, where a list of 10 words was presented three times, and the participants were asked to recall the words. Scoring of 0–30 was used to measure the total number of correct words learned (10-word recall) and scores of 0–10 were used to measure the correct words recalled after 5 min of distraction (10-word delayed) (Welsh et al., 1994). Experienced nurses, occupational therapists, and physicians at the memory clinics conducted testing.
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Assessment of Physical Fitness The SFT is a widely-used standardized and safe assessment for providing information about components of physical fitness in older people (Rikli & Jones, 2012). The SFT is a reliable test battery for assessing physical fitness in older people ≥ 60 years (ICC values 0.80–0.98) (Rikli & Jones, 2012), including those with MCI or early dementia (ICC values 0.93–0.98) (Hesseberg, Bentzen, & Bergland, 2015). According to those who developed the SFT, the test does not create a sum score for physical fitness level, but was designed to assess underlying physical components associated with functional mobility such as muscle strength, aerobic endurance, flexibility, body composition, dynamic balance, and agility (Rikli & Jones, 2012). The item scores create a profile of these fitness components associated with independent functioning (Rikli & Jones, 2012). Normative data based on age and sex for over 7,000 adults aged from 60 to 94 years from a population in the United States have been provided (Rikli & Jones, 2012). Scores between the 25th and 75th percentiles in each age and sex group (the middle 50% of the values) are defined as normal. Criterion-referenced fitness standards for maintaining physical independence in later years have also been developed for the SFT (Rikli & Jones, 2012). The cut-off scores for each age and sex group appear to be reasonable estimates of the level of fitness associated with remaining physically mobile and independent in later life (Rikli & Jones, 2012). Criterion standards have not been proposed for the two flexibility items, as there is insufficient evidence documenting the relationship between measures of flexibility and improved functional ability (Rikli & Jones, 2012). The SFT assessments were made in the following order: chair stand test for lower body muscle strength (number of repetitions within 30 s); arm curl test for upper body muscle strength (number of repetitions within 30 s); chair sit-and-reach test for lower body flexibility (distance between fingers and toes); back scratch test for upper body flexibility (distance between the third finger of each hand); 2.45-m up-and-go test (up-and-go) for agility and dynamic balance (time to rise, walk 2.45 m and return to the chair); and 6-min walk test to measure aerobic endurance (distance walked in 6 min). Height and weight were measured to calculate the BMI in kg/m2. More detailed descriptions are presented in the SFT manual (Rikli & Jones, 2012). SFT was assessed by an experienced physiotherapist (KH), and testing was conducted in rooms with adequate space and lighting in the hospitals where the subjects were recruited to ensure optimal performance.
Statistical Analysis Data are presented as the mean and standard deviation (SD) for continuous variables and as percentages for categorical variables. Differences between the groups, MCI and dementia, were tested
by the chi-square test and Fisher’s exact test for categorical data, and by independent sample t test for continuous data. Descriptive statistics with proportions were used to examine physical fitness scores for the study population compared with normative scores and with criteria used for measuring physical independence. Associations between physical fitness and cognitive performance were analyzed in a multiple linear regression analysis with the physical fitness parameters as dependent variables. Independent variables included the cognitive tests, MMSE, CDT, TMTA, TMTB, and the 10-word-list learning test, as well as the demographic factors of age, sex, education, and marital status. Statistically significant variables in the univariate analysis were included in a subsequent multivariate analysis. Backward removal analyses were used to analyze which cognitive domains (tests) were most related to the components of physical fitness. Bivariate correlations and analysis of multicollinearity were checked to detect any high level of association between independent variables and covariates. Residual plots were inspected, and if the model assumptions were violated, a sensitivity analysis was performed to test the robustness of the results. We considered p < .05 statistically significant. Statistical analyses were performed in SPSS for Windows version 20.0 (IBM Corp., Armonk, NY).
Ethics The study was approved by the Regional Committee for Medical Research Ethics in South-Eastern Norway. The participants were given oral and written information about the study and signed a written informed consent form before taking part. A physician at the memory clinic assessed whether the participants were able to give their consent before they were included in the study. The physicians considered the patient’s evidencing a choice, understanding, appreciation, and reasoning when they assessed the patient’s ability to participate. Our population consisted of older people with MCI and early dementia; at these stages of disease, consent is less problematic in comparison with more severe dementia. To prevent possible injuries or adverse events, the participants were followed closely during the assessments. They were asked if they needed breaks, and they were also instructed that they had the ability to withdraw from further testing and from the entire study at any time. No adverse events were recorded.
Results Of the 98 subjects, there were 45 men and 53 women; 60 were diagnosed with MCI and 38 with dementia. The participants with dementia (40% of the total sample) included Alzheimer’s disease (28%), vascular dementia (1%), and “other dementia” (e.g., dementia due to Parkinson’s disease, Lewy body disease, and frontal lobe dementia) (11%). The MCI diagnosis was not divided into subgroups. The mean age was 78.8 years, mean years of education was 13.5, and 40% were living alone (Table 1). In Table 1 more details regarding demographic characteristics are presented, as well as the scores for the components of the SFT and cognitive assessments of the study population. The demographic characteristics and scores on the SFT revealed no significant differences between MCI and dementia patients with the exception of years of education (p = .05). The MCI group had significantly better scores on four of the five cognitive tests compared with the dementia group. The performance level of the components of physical fitness (SFT) in our study group are compared with the normative data in the SFT and presented in Table 2. Our results show that the proportion of scores over normal was less than 25% in all of the parameters of
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Physical Fitness with MCI and Dementia 95
Table 1 Characteristics of the Participants All M (SD)
MCI %
M (SD)
Dementia
Variable
N
%
M (SD)
%
P-valuea
Gender (% women)
98
54
Diagnosis, MCI or dementia (% MCI)
98
61
52
58
.547
Living alone (% yes)
98
CSDD (% no symptoms, sum score < 6)
59
40
37
45
.426
48
53
40
.325
Age (years)
98
78.8 (7.4)
77.9 (7.2)
80.1 (7.6)
.151
Education (years)
82
13.5 (3.3)
14.0 (3.3)
12.6 (3.1)
.052*
MMSE (score 0–30)
98
24.1 (3.9)
25.5 (2.9)
21.8 (4.3)
< .001**
10-word recall (score 0–30)
95
12.3 (4.5)
13.4 (4.3)
10.6 (4.4)
.003**
10-word delayed (score 0–10)
94
1.9 (2.1)
2.2 (2.0)
1.4 (2.2)
.059
CDT (% normal, score 4–5)
98
51
60
37
.025*
98
3
0
8
.017*
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Cognitive assessment
TMTA, categorized (%) Unable to complete Score lower than –2 SD
36
32
42
Time between –1 and –2 SD
35
33
37
Time better than –1 SD
27
35
13
TMTB, categorized (%) Unable to complete
53
40
73
Score lower than –2 SD
97
13
13
14
Time between –1 and –2 SD
12
18
3
Time better than –1 SD
22
28
11
.005**
Senior fitness test Chair stand (# in 30 s)
98
9.4 (4.3)
9.3 (3.8)
9.6 (4.9)
.724
Arm curl (# in 30 s)
97
13.1 (3.8)
13.0 (4.0)
13.2 (3.6)
.779
Chair sit-and-reach (cm from fingers to toes)
97
–12.0 (12.6)
–11.8 (11.8)
–12.4 (13.8)
.822
Back scratch (cm between the third finger of each hand)
97
–16.4 (12.2)
–16.0 (12.8)
–17.1 (11.4)
.678
2.45 m up-and-go (s)
97
9.0 (3.7)
8.8 (4.1)
9.2 (3.1)
.580
6-min walk (meters)
90
420 (123)
434 (126)
399 ((117)
.196
97
23.8 (3.9)
23.8 (4.3)
23.9 (3.3)
.871
BMI
(kg/m2)
Abbreviations: MCI = mild cognitive impairment; CSDD = Cornell Scale for Depression in Dementia; MMSE = Mini-Mental State Examination; CDT = clock drawing test; TMTA = Trail Making Test A; TMTB = Trail Making Test B; BMI = body mass index. Significant differences between the patient groups (MCI and dementia) analyzed with Chi-square test, Fisher’s exact test, and independent-sample t test. *p < .05; **p < .01. a
the SFT, and that more than 25% of the participants had lower than normal scores in all of the parameters of the SFT with the exception of the arm curl test (Table 2). Table 3 presents the proportion of our study group having scores above and below the cut-off scores for the criteria for maintaining physical independence in later years. The four fitness items assessed showed that 68–85% of the participants had scores below the cut-off for predicting the ability to function independently in later years (Table 3). The results of multiple linear regression analyses regarding the associations between the components of physical fitness and cognitive domains in older people with MCI or dementia are presented in Table 4. The CDT was the only cognitive test significantly associated with lower and upper body muscle strength, represented by the chair stand test and the arm curl test. The associations remained statistically significant after adjusting for covariates (B = 1.75, p = .037
and B = 2.36, p = .002, respectively). The score on CDT was also significantly associated with the BMI after adjusting for covariates: a normal score on the CDT indicated a higher BMI (B = 2.07, p = .009). TMTB and CDT were significantly associated with dynamic balance and agility represented by the up-and-go test in univariate analysis, but TMTB was the only test that remained significant in the multivariate analysis (B = –0.64, p = .026). By inspecting the residual plots, we observed that the model assumptions were violated with the up-and-go test as the dependent variable. A sensitivity analysis was performed, with the same results. The 6-min walk test—representing aerobic endurance—showed a significant association with the TMTB, CDT, and 10-word-list recall in univariate analysis, but TMTB was the only test that remained significant in the multivariate analysis (B = 19.7, p < .001). Participants with better performance on the TMTB (shorter time to do the test) used
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96 Hesseberg et al.
Table 2 Senior Fitness Test Scores Compared with Normative Scores from a Population in the United States Above Normal Scores (%)
Normal Scoresa (%)
Below Normal Scores (%)
Chair stand (# in 30 s)
4
50
46
Arm curl (# in 30 s)
8
67
18
Chair sit-and-reach (cm from fingers to toes)
2
40
56
Back scratch (cm between the third finger of each hand)
11
45
43
2.45 m up-and-go (s)
2
43
6-min walk (meters)
7
58
n = 98 Item
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Significant Variables from Univariate Analysis
p-value
95% CI
R2
Age
–0.14
.015*
–0.25 to 0.03
.12
Clock drawing test
1.75
.037*
0.11 to 3.40
Age
–0.12
.018*
–0.22 to –0.02
55
Clock drawing test
2.36
.002**
0.92 to 3.81
36
Trail Making Test B
0.38
.275
–0.31 to 1.07
Age
0.16
.001**
0.07 to 0.26
Trail Making Test B
–0.64
.026*
–1.21 to –0.08
Clock drawing test
–0.92
.273
–2.58 to 0.74
Age
–6.9
< .001**
Trail Making Test B
19.7
.044*
0.52 to 38.41
Clock drawing test
1.07
.970
–55.71 to 57.86
10-word-list recall
2.59
.378
–3.22 to 8.40
Clock drawing test
2.07
.009**
0.53 to 3.61
Age
–0.09
.102
–0.20 to 0.02
Table 3 Senior Fitness Test Scores Above and Below Cut-off Scores for Recommended Fitness Standards for Predicting the Ability to Function Independently in Later Yearsa
a
Multivariate Analysis Ba
a Normal scores are defined as those between the 25th and 75th percentiles in each age and sex group (the middle 50% of the values).
Above Cut-Off Scores (%)
Below Cut-Off Scores (%)
Chair stand (# in 30 s)
23
77
Arm curl (# in 30 s)
32
68
2.45 m up-and-go (s)
15
85
6-min walk (meters)
27
73
n = 98 Item
Table 4 Associations Between Physical Fitness Items and Cognitive Assessments, Adjusted for Demographic Factors in a Multivariate Analysis
Fitness standards according to Rikli and Jones (2012).
less time to perform the up-and-go test (0.64 s less for each category improvement) and walked longer on the 6-min walk test (19.7 m longer for each category improvement). The chair sit-and-reach and back scratch items, both measuring flexibility, showed no significant association with any of the cognitive tests. The cognitive tests MMSE, TMTA, and the 10-word-list recall and delayed test showed no significant association with the components of physical fitness in the univariate analysis. The only exception was a significant association between the 10-word-list recall and the 6-min walk test in univariate analysis, but not in the multivariate analysis.
Discussion In this study we explored the performance level of the components of physical fitness in older persons with MCI or dementia and examined the relationship between the components of physical fitness and different aspects of cognition in community-dwelling older people with MCI or dementia. Overall, the study demonstrated that the older people recently diagnosed with MCI or dementia showed a lower level of physical fitness on all of the physical fitness items except the arm curl test when compared with the normative data of the SFT (Rikli & Jones, 2012). Criteria to predict the ability to function independently in later years were provided for the SFT (Rikli & Jones, 2012), and a high proportion of the participants (68–85%) in this study scored below these cut-off scores. Furthermore, significant associations between physical fitness and cognition were found in
Chair stand test (n = 98)
Arm-curl test (n = 97) .18
Up-and-go (n = 97) .17
6-min walk (n = 86) –10.25 to –3.64 .23
Body mass index (n = 97) .07
Note. Demographic factors in the univariate analysis included age, sex, marital status, and years of education. Sex was included in the multivariate analysis but was not significant in any of the analyses. Cognitive assessments in the univariate analysis: Mini-Mental Status Examination, 10-word-list recall and delayed test, Trail Making Test A, Trail Making Test B, and clock drawing test. a B = unstandardized coefficient. *p
