Abstract
INTRODUCTION
People with Parkinson’s disease (PD) often become less active in everyday life over time, especially as disease advances. A more sedentary lifestyle dominated by sitting or lying is problematic because it is associated with muscular weakness, osteoporosis, and increased risk of cardiovascular disease [1]. Moreover, a sedentary lifestyle has been associated with falls in senescence [2]. In PD, prospective studies have reported prior falls in the preceding year, postural instability and gait difficulty (PIGD), freezing of gait and fear of falling as important risk factors for falling [3, 4, 3, 4]. In addition to fall-related injuries, the consequences of recurrent falls include more need for health care services, suggesting a complex relationship between falls, sedentary behavior and ambulatory activity [5].
Sedentary behavior and ambulatory activity can be viewed as independent functions and demonstrate independent risk factors [6]. Knowledge about sedentary behavior and ambulatory activity among people with PD in real life settings is scarce. In a recent study, the pattern (distribution) but not the volume of sedentary behavior was different in people with advanced PD versus controls [7]. Another study reported that objectively measured volume of daily ambulatory activity (accelerometer-based data monitored over 7 days) was reduced in early PD compared with controls, and that patterns of ambulatory pattern were also different [8], indicating the subtlety of this measurement approach. Furthermore, the number of steps and intensity of ambulatory activity in people with PD declined in a 1-year follow-up study [9], and the percentage of total time spent walking in people with PD improved after a home cueing training program [10], leading to the assumption that ambulatory activity is rapidly influenced by the disease and management of symptoms.
To date, only two studies have examined the relationship between selected aspects of physical activity and falls in PD. The first study reported that falls occurring during changes of posture (such as rising from a chair) were associated with reduced levels of ambulatory activity [11], whereas the second study showed that quality of gait but not quantity differed between fallers and non-fallers [12]. This study extends previous work by comprehensively examining physical activity and falls, and as such had two aims. The first aim was to quantify the volume, pattern and variability (accelerometer-based data monitored over 7 days) of sedentary behaviour, standing and ambulatory activity in people with PD with and without recent fall history; and second, to examine the role potential mediators (demographics, motor impairment, fear of falling, mobility and dementia) have on the volume of sitting/lying, standing and ambulatory activity in people with PD with and without recent fall history. We hypothesized the following: i) the volume of ambulatory activity would be similar among participants with and without a fall history in contrast to findings in older adult cohorts [2]; ii) fallers would be more sedentary as a result of spending less time standing; and iii) the volume of sedentary behaviour and standing would be influenced by different factors in participants with and without a recent fall history.
METHODS
Participants
Fifty people with PD nested within the ongoing Norwegian ParkWest study were recruited for this pilot study conducted between February 21, 2013 and June 24, 2014. The Norwegian ParkWest study is a multicenter, prospective population-based cohort study of the incidence, neurobiology and prognosis of PD. The study protocol is described in detail elsewhere [13].
In brief, multiple sources of case ascertainment and a four step diagnostic procedure were used to establish a representative cohort of patients with incident PDat a high level of diagnostic accuracy within four Norwegian counties. For the present study, we aimed to recruit ParkWest participants with PD from the two centers with the largest populations (Rogaland and Hordaland). The participants were categorized as fallers if they had one or more falls (an event which results in a person coming to rest inadvertently on the ground) during the past 6 months, and the recruitment continued until the falling and non-falling groups were comparable sized and matched for age and sex. Participants unable to consent or wear an accelerometer were excluded. The study was approved by the Regional Committee for Medical and Health Research Ethics, Western Norway (Ethics number 2010/1700). Signed written consent was obtained from all participants.
Procedures
Information regarding sociodemographic variables and mobility was obtained during a structured interview. Mobility capability was assessed in terms of need for help during ambulation (walking aid) and confidence in being able to get up from floor unaided (yes/no). Level of concern about falling during social and physical activities inside and outside the home was measured using the Falls Efficacy Scale-International (FES-I) [14]. Severity of motor impairment and disease stage was assessed by the Unified Parkinson’s Disease Rating Scale (UPDRS) motor section (part III) [15] and the Hoehn and Yahr scale [16] by trained neurologists experienced in movement disorders. Disease duration was determined as the time period between motor onset (recalled by the participants at the time of diagnosis)and the time of assessment. Participants with a recent fall history were asked about details concerning fall events, such as environmental and behavioral circumstances and their own considered main opinion as to why they had fallen. A diagnosis of PD dementia (PDD) was determined according to published criteria [17], as described in a previous study from this group [18]. Participants with clinically significant cognitive impairment were accompanied by caregivers. All participants met the United Kingdom PD Society Brain Bank diagnostic criteria [19] and were examined after median 9 (7–14) years of PD duration.
Body posture and ambulatory activity were monitored in real life settings with the validated accelerometer activPAL3 TM (PAL Technologies Ltd., Glasgow, UK) for 7 days [20, 21]. The activPAL3 TM is a small (35×53×7 mm) and lightweight (15 g) device with a sampling frequency of one reading of acceleration every 1/20th of a second, which senses and records sitting/lying (sedentary behavior), standing and steps (ambulatory activity). Once programmed for overall wearing time, the device was applied a waterproof attachment (nitrile sleeve for activPAL3 TM and 3M Tegaderm transparent dressing) and attached on the mid-line of the thigh least affected by Parkinsonism, in the lower part of femur, one third of the way between hip and knee. The participants were instructed to remove the device only during bathing and were provided with replacement dressing to re-attach the device if necessary. Upon completion of recording, the device was removed in the clinic or posted back to the researcher as convenient for the participants. To be included in the analyses, participants had to wear the accelerometer at least 4 days.
The activPAL 3TM software package processes the acceleration measures by using proprietary algorithms to produce a record of three activity events: sedentary behavior (sitting or lying), standing and ambulatory activity. Data from activPAL3 TM were exported to Excel (Microsoft Corp., Redmond, WA, USA) for further analysis. A bespoke MATLAB® program extracted bouts of (i) sedentary behavior, (ii) standing and (iii) ambulatory activity, and computed the followingoutcomes: Volume: percentage of time and total number of sedentary, standing and ambulatory bouts per week. Pattern (alpha, α), a unit-less parameter which is derived from a power distribution of bouts of activity, where a lower α for ambulatory behavior indicates a distribution derived from greater proportion of long bouts [22]. Variability, the within subject variability (seconds) of bout length was calculated using a maximum likelihood technique due to a log-normaldistribution, where a high variability figure indicates a more varied length of bout [23]. The lengths of bouts by strides in three different durations were identified in a period of 7 days and described as total number of strides occurring in bouts of low duration (<10 strides), medium duration (10–50 strides) and long duration (>50 strides) [24].
Statistical analysis
Comparisons between groups were performed using Mann-Whitney U tests for continuous variables and Chi square or Fisher’s exact test for nominal variables as appropriate. P values < 0.05 were considered to be statistically significant. Assumptions of multiple regressions (normality, linearity and homoscedasticity) were examined in scatterplots of predicted values against residuals. The Shapiro-Wilk test performed on dependent variables indicated non-normality of total ambulatory time. Therefore, a square root transformation was applied on this variable according to the underlying assumptions. Presence of multicollinearity was determined using cut-off points of tolerance value < 0.10, or variance inflation factor above 10. Standard regressions were used to study explanatory variables that contributed significantly to total time sedentary, standing, and ambulatory by calculating adjusted explained variance (R2) and standardized coefficients (β). We initially conducted univariate linear regression, and followed this up by entering variables with a P value < 0.05 into multivariate models. Due to the high intercorrelation between UPDRS motor score and Hoehn and Yahr stage, we only included the variable with the highest standardized β value into multivariate linear regression analysis. The ratio of cases to independent variables was evaluated using N≥20 + 5 m (where m is the number of independent variables) in the multivariate models [25]. All analyses were performed in IBM SPSS Statisticsversion 22.
RESULTS
Sample characteristics
Of 50 people with PD recruited for this study, 2 were excluded due to missing data (one device was lost and the other had fallen off within the first 4 days of wearing without being reattached). Therefore, 48 participants were eligible for further analyses. Mean wearing time was 7 days. The participants spent averagely 75.7% of their time sedentary, 19.6% standing and 4.7% of their time ambulatory. Among participants, 20 (41.7%) reported one or more falls and 28 (58.3%) had not experienced a fall during the last 6 months. Participants considered the main reason for one or more falls in the preceding 6 months to be; lower extremity muscle strength/unable to react fast enough (25%), freezing of gait/shuffling (20%), did not know (20%), symptomatic orthostasis (15%), not paying attention (10%), sensory impairment in lower extremity (5%), and hallucinations (5%). Half of participants falling reported that they usually had an accident due to freezing of gait, shuffling, difficulties with stairs or uneven floor tiles and bricks. Table 1 shows that participants with a fall history had higher Hoehn and Yahr stage, reported more fear of falling, and used walking aids more frequently than those who did not fall. Outcomes from the activPAL3 TM accelerometer showed that participants who reported falling spent more time sedentary and less time standing compared with non-falling participants, whereas total ambulatory time was similar between groups.
Linear regression models of total time sedentary, standing and ambulatory
Table 2 shows the results of the regression models.Age, sex, living with a partner, education, UPDRS motor score, Hoehn and Yahr stage, FES-I, confidence in being able to get up from floor unaided, walking aid, and PDD were included as independent variables in univariate linear regression analyses for participants with and without a fall history separately for the three dependent variables. The overall variance explained for fallers in multivariate models ranged from 42.4–54.8% , and for non-fallers from 30.6 –46.5% . Confidence in being able to get up from floor unaided was the unique contributor to reduced total time sedentary (β = –0.489) and increased time ambulatory (β = 0.434) in multiple regression analyses for participants with a fall history. Among participants without a fall history, higher UPDRS motor score contributed significantly to increased total time sedentary (β = 0.433) and reduced time standing (β = –0.379), whereas higher Hoehn and Yahr stage contributed significantly (β = –0.564) to reduced total time ambulatory.
DISCUSSION
The key finding from this study was that participants with PD who reported retrospective falls in the last 6 months were more sedentary because they spent less time standing than non-falling participants. Reasons for this are not entirely clear, but reduced time in standing may be a safety strategy to compensate for disease severity. There were no differences in more nuanced measures of physical activity such as total number of sedentary bouts or differences in measures that reflect the pattern and variability of sedentary behaviour, standing or ambulatory activity which is surprising, although we did observe a trend (P = 0.06) for participants who reported falling to demonstrate less varied length of standing bouts. Findings from the regression analyses showed that confidence in being able to get up from the floor unaided and less disease specific motor symptoms were strongly associated with an active lifestyle in participants with and without a recent fall history, respectively. To our knowledge, this is the first study to compare objectively measured sedentary behaviours, standing and ambulatory activity in a matched PD cohort with and without fall history. As such, our findings may have implications for the management of people with PD who have fallen, including advice and practicing getting up from the floor and how to safely perform activities of daily living during changes in posture.
The average volume of sedentary behavior (75.7%) and walking time (4.7%) found in our PD group is similar compared with previous work [7, 8]. Although results should be interpreted with caution due to the moderately small sample size, the volume of standing time has not been previously reported in people with PD. Examining differences between participants with and without a recent fall history with detailed data from the accelerometer, we found comparable volumes of total ambulatory activity as earlier reported [11, 12]. We extended these findings by examining the number of ambulatory bouts per week and number of strides occurring in bouts of different durations, although did not find significant between- group differences. Increased volume of sedentary behavior in participants with a recent fall history has not been demonstrated in PD, but has been reported in community-dwelling older men identified as recurrent fallers [2]. The increase in sedentary behavior we observed corresponded to a significant reduction in standing rather than a reduction in ambulatory activity, as we hypothesized. It is possible that time spent standing was replaced by time sitting as a safety precaution, consistent with our findings of more severe motor symptoms, frequent use of walking aids and fear of falling among participants with a fall history.
Although we did not find strong evidence for the associations between different patterns of activity and sedentary behavior on falls, earlier work has reported this as a feature of disease. Compared to controls, people with PD walk in bouts of shorter duration [8] and are sedentary in bouts of longer duration [7]. A longitudinal study design or a more sensitive monitor may capture differences with respect to falls more effectively. For example, a recent study demonstrated that PD fallers had increased gait variability, less consistent gait pattern and less smooth gait compared to non-falling people with PD, using a more sensitive (100 Hz) accelerometer [12]. However, short walking episodes (<60 seconds) or quantified standing and sedentary behavior were not included in the analyses, and direct comparisons are difficult as our study used more standard methods for measuring ambulatory pattern compared to analyses of raw acceleration signal displayed as the amplitude, width and variability within the frequency spectrum.
Interestingly, the potential mediators of increased sedentary behaviour and reduced ambulatory activity in the multivariate analysis were somewhat diverging comparing those with and without a recent fall history. As expected, sedentary behaviour, standing and ambulatory activity were highly correlated with the severity of motor symptoms in both groups. However, the associations between less time spent sedentary and increased time spent ambulatory with confidence in being able to get up from floor unaided were unexpectedly strong among participants who had fallen. Potential explanations include experienced difficulties during daily activities, including rising from a lower level, or more likely, how participants perceive their overall mobility. Noteworthy, in the univariate linear regression models PDD influenced negatively on the ability to retain an active lifestyle among participants who had fallen and was associated with less ambulatory activity among non-fallers. However, in the multivariate analyses PDD did not contribute significantly to the amount of any of the activities. This finding may indicate a complex interaction between fall, attitude, environment, comorbidity and the ability to retain an active lifestyle. Interestingly, a recent meta-analysis showed that sedentary behaviour increased the risk of depression by up to 25% in adults [26], suggesting that aspects of personality, anxiety and coping should be further examined in future studies of sedentary behaviour and falls in PD.
Limitations of this study include the cross-sectional design, the relatively small sample size and the retrospective assessment of fall history rather than prospective, monthly reporting which is the gold standard [27]. Instead, we asked participants about details concerning fall events, such as environmental and behavioral circumstances and their own considered opinions as to why they had fallen, which have been reported to be memorable and easily recalled [28]. Despite the link between confidence in being able to get up from the floor and total time spent sedentary and ambulatory in participants with fall history, we were unable to establish causation between falls and changes in physical activity. The strengths of our study include objectively measured outcomes of sedentary behavior, standing and ambulatory activity in real life settings, as well as matched groups of people with PD, the latter allowing us to control for age, sex and motor severity to examine potential mediators of real life activity across the categories of fall history.
The potential unintended and harmful consequences of immobility can contribute to deconditioning. This fact underscores the importance of retaining an active lifestyle. Although the results should be interpreted with caution due to the moderately small sample size, our study indicates that more emphasis should be taken to reduce sedentary behavior in people with PD. In general, encouraging routine strength and balance training, changes in environment, attitude or behavior should be a priority in people with PD who adopt a more sedentary lifestyle [29]. More specific, improving confidence in being able to get up from the floor unaided and maintaining the ability to perform activities of daily living during changes in posture might be important barriers to target. This strategy not only could enhance an active lifestyle, but may also improve quality of life and independent living.
Conflict of interests
Hiorth, Larsen, Lode, Lord and Pedersen declared no relevant conflicts of interest with respect to the authorship or publication of this article. Tysnes has been invited speaker for GSK, Orion Pharma, Pfizer, UCB, Novartis and Lundbeck and has participated in an advisory board for Lundbeck. Godfrey has been supported by the Biomedical Research Centre (BRC) and Unit (BRU). Rochester’s research program has been supported by grants from MRC, NIHR HTA, NIHR BRU, Parkinson’s UK, EH Framework 7. Rochester has received honoraria from USB, Teva andLundbeck.
Footnotes
ACKNOWLEDGMENTS
Hiorth has received research support from the Norwegian Parkinson Disease Association. The Norwegian ParkWest study was supported by grant # 9111218 from the Western Norway Regional Health Authority, grant # 177966 from the Research Council of Norway and the Norwegian Parkinson Disease Association. The authors are grateful to all participants for their willingness to participate in this study and thank all personnel involved in planning and conducting the Norwegian ParkWest study.