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An Exploration of Falls and Dual Tasking

A Prospective Cohort Study of People With Multiple Sclerosis

Quinn, Gillian BSc (Physiotherapy); Comber, Laura BSc (Physiotherapy); O' Malley, Nicola BSc (Physiotherapy); McGuigan, Chris MD; Galvin, Rose PhD; Coote, Susan PhD

doi: 10.1097/TGR.0000000000000234
Aging With a Progressive Neurologic Disease
Free

Objective: To explore the relationship between dual-task cost and falls in people with multiple sclerosis.

Methods: One hundred participants completed a falls screening questionnaire, Timed Up and Go (TUG), and TUG-Cognitive (TUG-C) at baseline. Dual-task cost was the percentage change in performance between TUG and TUG-C. Falls were recorded prospectively for 3 months.

Results: Dual-task cost was not associated with increased risk of falls (P = .90, odds ratio = 1.00). Answering yes to a question about problems doing 2 things at once increased likelihood of falls (risk ratio = 2.07).

Conclusion: A single question asking about dual tasking may be a useful screen for falls risk assessment.

School of Allied Health, University of Limerick, Limerick, Ireland (Mss Quinn, Comber, and O' Malley); Physiotherapy Department (Ms Quinn), St Vincent's University Hospital, Dublin, Ireland (Dr McGuigan); and School of Allied Health & Health Research Institute University of Limerick, Limerick, Ireland (Drs Galvin and Coote).

Correspondence: Gillian Quinn, BSc (Physiotherapy), School of Allied Health, University of Limerick, Limerick, V94 T9PX, Ireland (Gillian.Quinn@ul.ie).

Both Gillian Quinn and Laura Comber are in receipt of funding from the Multiple Sclerosis Society of Ireland, MS Ireland. None of the other authors have any conflict of interest to declare.

Accidental falls are well known to be prevalent in older people; however, people aging with multiple sclerosis (MS) experience a rate of accidental falls that far exceeds that of healthy populations older than 65 years. In any 3-month period, 50% of people with MS sustain a fall.1 When examining falls specifically among middle-aged and older adults with MS, 64% of the study sample reported at least 2 falls each year2 and factors associated with an increased falls risk in people aged 45 to 90 years with MS include problems with balance or mobility and poor concentration or forgetfulness.3 The serious consequences of falls such as physical injury, increased care needs, and further physical deconditioning as a result of activity limitation secondary to fear of falling are far reaching with a high socioeconomic associated cost.4,5 People with MS are commonly diagnosed in their thirties and thus may be living with the condition for 40 to 50 years as MS does not affect life expectancy unless disability is severe.6,7 People aging with MS will have to endure normal age-related changes in their health as well as having to cope with MS-related disability and disease progression.8 Indeed, many symptoms of the natural ageing process such as decreased muscle strength, sensory and visual impairment, and problems with balance, vision, and cognition are all overlapping symptoms in MS9 and mean that relatively “young” people with MS will present with problems similar to older adults.

Two of the most common symptoms of MS include motor dysfunction and a decline in cognitive ability.10 Difficulty walking has been reported as a significant symptom by up to 67%11 of people with MS and even in the early stages of the disease, significantly altered gait patterns are evident in comparison with their healthy peers.12 Notably, middle-aged cohorts13 have demonstrated reduced walking speeds similar to that of a healthy sample of 70 to 80 years of age.14 Similarly prevalence of cognitive impairment has been reported to be present in up to 70% of people with MS,15 presenting early in the disease course and deteriorating over time.16 Limitations in mobility and cognitive functioning are both associated with falls in older people17,18 and similarly the association of both walking limitations and cognitive factors with falls is confirmed in a recent systematic review of falls risk factors in MS.19 Among middle-aged and older adults with MS interviewed about their falls experience, expected causes of falls such as balance and lower limb impairment were reported in 41% and 31% of cases, but interestingly cognitive factors were reported as a cause of falls in 17% of cases.20

These 2 factors of impaired cognition and impaired mobility together underlie the principle of cognitive motor interference (CMI), which is common in MS21 and refers to the decline in performance of cognitive and/or motor tasks when they are performed simultaneously (dual task), relative to the performance of each task individually.22 The deterioration in performance associated with CMI is expressed as dual-task cost (DTC)23 and has been shown to be associated with falls in older people.24 However, there is a scarcity of studies looking at the association of DTC and falls risk using prospective falls recording in people with MS. Previous research demonstrated conflicting results, with 1 study reporting that DTC is not related to falls status,25 while another more recent study found that DTC is associated with an increased risk of recurrent falls in a 6-month period (odds ratio [OR] = 1.23, confidence interval [95% CI] = 1.02-4.45).26 In studies of older people simply asking about fear of falls and their confidence in doing certain activities have been shown to be associated with falls risk27,28 but their perceived ability to do 2 things at once in relation to falls risk has not been fully explored. Similarly, in MS, self-report problems with dual tasking and its potential association with falls risk have not been examined. In a recent review examining patterns of CMI poststroke, a categorization framework that identifies 9 possible patterns of CMI during a cognitive-motor dual task was presented.22 The patterns of CMI discussed include no interference, cognitive-related motor interference, mutual interference, and mutual facilitation among others. No research to date has examined the patterns of CMI in people ageing with MS and whether the use of any specific pattern is protective or predictive of falls.

Given the current shortage of prospective cohort studies examining DTC and CMI and their potential association with falls risk in the older MS population, the primary objective of this study was to explore the extent of CMI in fallers and nonfallers and investigate the difference between them by measuring it objectively as DTC percentage and subjectively as a yes/no question asking about difficulty doing 2 things at once. We further aimed to investigate the ability of objective and subjective measures of DTC and CMI to predict falls status using OR and risk ratio. Finally, we aimed to describe the different CMI patterns used among people with MS and examine their association with fall status.

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METHODS

Design

This was a prospective cohort study and as this is an observational study, we followed the STROBE (STrengthening The Reporting of OBservational studies in Epidemiology) Statement guideline.29 The study was approved by the University of Limerick Ethics Committee and the St Vincent's Healthcare Group Ethics and Medical Research Committee.

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Recruitment and eligibility

Consecutive patients attending a tertiary referral MS clinic at St Vincent's University Hospital, Dublin, were invited to participate in the study if they met the following inclusion criteria: (1) A neurologist confirmed diagnosis of MS as per 2010 McDonald Criteria,30 (2) an Expanded Disability Status Scale score of between 3 and 6.531 indicating that they had some walking limitations but were still able to ambulate independently (with or without a mobility aid), and (3) adequate cognitive function to participate in the assessment and fill out falls diaries for the 3-month study period. Participants younger than 18 years, pregnant woman, or individuals unable to provide informed consent were excluded from the study. Recruitment and participant assessment were carried out between November 2014 and March 2016 with the final falls diaries collected in June 2016.

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Baseline measures

Demographic information, MS classification subtype, Expanded Disability Status Scale score, and disease duration were recorded from the medical records during the baseline assessment. Consenting participants then completed a falls screening questionnaire, which included yes/no questions about fear of falls, use of a mobility aid, history of falls in past 3 months, and problems doing 2 things at once among others. The questionnaire items were based on a review of the literature on factors associated with and predictive of falls in MS. Participants then completed the objective measures, the Timed Up and Go (TUG), under single- and dual-task conditions. The TUG has been shown to be a valid measure of functional mobility in MS patients32 with good construct validity when assessing walking and balance performance among people with MS.33 Previous research found that more than 80% of falls in the MS population occurred during transfers, while 60% occurred during walking.34 The TUG incorporates both types of mobility task, so its face validity appears good in relation to determining falls status and it has been previously used to assess dual-task ability in people with MS.35

The TUG-Cognitive (TUG-C) was performed after the TUG and consisted of the participant completing the same mobility test, while simultaneously performing a cognitive task. For this study, the cognitive task consisted of serial subtraction in multiples of 3 from a randomly chosen number between 20 and 100. Serial subtraction was selected as it has a stable cognitive load throughout the duration of the test.36 Dual-tasking ability was also measured subjectively as individuals were asked about their self-perceived dual-tasking ability as part of the falls screening questionnaire: “Do you have problems doing two things at once: yes, or no?.” The measures were performed in the same standardized order for every participant and participants were advised to walk as quickly and safely as possible while in their usual footwear and using their usual mobility device (if applicable). The participant was seated in a standard height chair with his or her back against the chair and was then instructed to stand up, walk 3 m to a specific mark on the ground, turn around, and walk back and sit in the chair again. Timing began when the participant started to rise from the chair and ceased when he or she was seated in the chair after walking back. The participant had 1 practice trial and then 3 recorded trials, with a mean value of the 3 walks used for statistical analysis.

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Dual-task cost

Dual-task cost was calculated using the previously published equation, where ST = single task and DT = dual task37:

Therefore, for this study, DTC was calculated and expressed as a percentage, with a larger percentage change value indicating a worse performance, with the following equation:

To determine the patterns of CMI, 3 assessors (2 physiotherapists with 20 and 3 years of experience, respectively, and a final year physiotherapy student) observed the pattern of interference during the TUG-C of the first 12 participants. Following this, the assessors met to agree on categories, with 6 different patterns identified. The pattern of the remaining participants was recorded on the basis of their use of 1 of the following 6 patterns:

  • Pattern 1: No changes in gait, numbers correct
  • Pattern 2: No changes in gait, numbers incorrect
  • Pattern 3: Changes in gait, numbers incorrect
  • Pattern 4: Stop, think, and say number, take step
  • Pattern 5: Synchronize step and think
  • Pattern 6: Changes in gait, numbers correct
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Falls

Falls incidence was calculated using prospective falls diaries for a 3-month period, as recommended by the International MS Falls Prevention Research Network38 where participants recorded whether they had a fall and the number of falls per day. A fall was defined as “an unexpected event in which you come to rest on the ground, floor, or lower level.”39 The participants were provided with stamped self-addressed envelopes and falls diaries to be returned monthly. Those not returning their diaries were contacted by the researcher to remind them or to collect the data for that month by phone. Participants also had the option of a text or e-mail reminder to be sent fortnightly to optimize falls reporting. Consistent with other studies of this type, a faller was classified as a person with 2 or more falls.25,26

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Statistical analysis

All data collected were coded and inputted into an Excel spreadsheet and then analyzed using SPSS (Version 22). Normality of distribution was assessed using the Kolmogorov-Smirnov test. Descriptive statistics and t tests or Mann-Whitney U tests, as appropriate, were used to compare demographic characteristics between groups at baseline and to compare outcome measures postassessment. Chi-square tests were used for categorical variables. All data were presented as mean (standard deviation), median (interquartile range), or proportion accordingly. The relationship between objective measurement of DTC and fall status was assessed using binary logistic regression to have a comparative methodology to previous studies on this topic.25,26,40 Chi-square test was used to assess whether self-reported problems with dual tasking and pattern of CMI were different between the groups based on falls status. Risk ratio was calculated for subjective problems with dual tasking and for the various patterns of CMI. Missing data were excluded on analysis-by-analysis basis. The significance level for all statistics was set at P ≤ .05.

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RESULTS

Participant characteristics

A total of 101 participants were recruited for this study, with falls data collected for 100 individuals. One participant withdrew from the study after the baseline assessment as he or she felt uncomfortable filling out the monthly falls diaries. A total of 791 falls were reported by 56 participants over the 3-month reporting period, with 34 of these individuals having 2 or more falls and meeting our criteria for faller classification. There was a diary return rate of 99.7%. In the faller group, the number of falls ranged from 2 to 164 per faller, with a mean number of 22.6 (SD: 45.4) falls. Demographic information and clinical characteristics of the recruited participants are displayed in Table 1.

TABLE 1

TABLE 1

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Primary outcome—DTC

Objective measure of DTC (percentage change between the TUG and the TUG-C)

For the whole cohort of N = 100, the median DTC was −13.19, interquartile range: 21.60 (thus, a 13% deterioration under dual-task conditions as measured by the TUG and the TUG-C). The range in DTC was from −169.30 to 12.42, indicating that some participants improved under dual-task conditions and had a faster TUG-C than their TUG time (14 participants in total). The majority of participants, 86%, showed deterioration in mobility performance under dual-task conditions, with 46% of the total group demonstrating a change in DTC of greater than 15%, of whom 32.6% were fallers. No significant difference was found between the DTC of fallers and nonfallers (Table 2). Binary logistic regression on the association between DTC and odds of falls was not significant (OR = 1.00, 95% CI: 0.98-1.02, P = .90).

TABLE 2

TABLE 2

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Subjective measure of DTC (yes/no question about difficulty doing 2 things at once)

A significantly higher percentage of fallers (65%) subjectively reported problems with dual tasking during their initial assessment compared with nonfallers (P = .01), Table 3. The risk of falling was doubled if the participants reported problems with dual tasking with an associated risk ratio of 2.07 (95% CI: 1.15-3.71).

TABLE 3

TABLE 3

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Patterns of CMI

Analyses on pattern of CMI were performed for the 88 participants who had that data (Table 4). Differences between fallers and nonfallers were significant for those using pattern no. 6 (changes in gait, numbers correct) (P = .03). An increased risk of falling was highest for those using pattern no. 6 (RR= 1.82, 95% CI: 1.09-3.04), where RR is the risk ratio which is the ratio of the probability of an outcome in an exposed group to the probability of an outcome in an unexposed group, and those using pattern nos. 1 and 2 had a protective effect and were more likely to be nonfallers. As seen in the Figure, the most commonly used patterns among the whole group were no. 3 (changes in gait, numbers incorrect) and no. 6 (changes in gait, numbers correct). The least common pattern was no. 5 (synchronize step and think), which involved the participant taking a step at the same time as saying the number.

TABLE 4

TABLE 4

Figure

Figure

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DISCUSSION

The primary objective of this study was to investigate whether objectively measured DTC, calculated as the percentage change between the TUG and the TUG-C, was associated with falls status in people with MS, and the results suggest that there is no association. The subjective measure of DTC examined by asking the question “Do you have problems doing two things at once?” showed a significant difference between fallers and nonfallers and demonstrated that participants who report problems dual tasking are at twice the risk of falling when compared with those without problems dual tasking. Six distinct patterns of CMI were identified among this cohort of older people with MS and there was a significant difference between fallers and nonfallers and an increased risk of falls for those using pattern no. 6 (changes in gait, numbers correct). As the mean age of this study cohort is 52.6 years, they are already starting to experience the natural processes that occur with ageing and affect one's strength and mobility such as decreased muscle mass, decreased coordination, slower speed of movement, and increased movement variability.41 Overall, the age-related changes in the musculoskeletal system will be heightened in this MS cohort who already have dysfunction of the central and peripheral nervous system affecting mobility and activity performance, with falls being just one of the detrimental consequences. Problems such as falls and their sequela become more severe as the person with MS ages and these difficulties have been shown to be age related and age accelerated.42

The findings of this study regarding objectively measured DTC and falls status are consistent with previous findings from a comparable study population that similarly used a change in gait velocity during a mobility assessment to measure DTC.25 Another more recent prospective study that also used change in gait velocity to measure DTC but with a study population with relapse-remitting MS only and a milder disability level additionally found that DTC was unable to predict future falls.40 In contrast to these findings, a study using static posturography and electronic walkways found that the DTC of both cognitive performance and walking velocity was associated with an increased risk of recurrent falls among people with MS.26 However, the latter study had some noteworthy methodological differences when compared with the other studies. The study population was younger with a shorter disease duration and had significant methodological differences using more detailed and objective measures in the form of static posturography for balance assessment, electronic walkway for gait assessment, and correct response rate (response rate per second multiplied by percentage of correct responses) as the measure of cognitive performance whereas the other studies including this one used only simple timed walks when assessing DTC. However, it is often the more simple measures that can be easily performed without the use of expensive equipment that translate across to everyday clinical practice.

Our finding that DTC does not predict falls in MS differs to those of studies examining this concept in other populations. A study of more than 1000 older adults found that an objectively measured DTC of 18% or more prospectively predicted fallers (OR = 1.07; 95% CI: 1.04-1.10),43 but a recent systematic review has concluded that further prospective studies of older adults are needed to develop recommendations for dual-task testing as part of a multifaceted falls risk assessment.44 In subacute stroke patients, dual-task assessment of gait has demonstrated an altered stride length and step length in fallers versus nonfallers,45 and a longitudinal study of people with Parkinson disease demonstrated that motor DTC significantly predicted future fallers with a sensitivity of 71%, specificity of 77%, and 2.6 higher odds of being a future faller.46 A prospective study examining prediction of falls and near falls in people with mild Parkinson disease included a subjective question about dual tasking similar to our self-report measure of problems dual tasking, and simple logistic regression showed a self-report of balance problems while dual tasking had an OR of 4.0 for predicting falls and/or near falls.47

To the knowledge of the authors, this is the first study that investigated whether self-reported problems with dual tasking were linked to falls status in people with MS. Previous research among older people with MS has asked about problems with concentration and forgetfulness2,3 and qualitative interviews have identified situations that require divided attention as a factor related to falls,48 but no research to date has specifically asked about the participant's difficulties in doing 2 things at once. This concept of asking a simple question to help identify falls risk has been previously demonstrated in MS with regard to history of falls49 and in older people where health professionals are advised to routinely ask simple questions about fall history, fear of falls, and feelings of unsteadiness as a quick falls risk screening tool.50 In this study, a significant difference was identified between fallers and nonfallers in relation to subjectively reported problems with dual tasking. One possible reason for this finding may be that when individuals are subjectively reporting problems with dual tasking, they are considering all dual tasks that occur in their daily routine, whereas objective measures of dual-tasking ability look only at 1 dual-task activity in a controlled setting. A recent review21 determined that most dual-task tests in the MS population were conducted at a self-selected speed, similar to the task in this study. However, it is suggested that these tests are not representative of activities of daily living, when people are more likely to be carrying out tasks at a heightened speed and in novel environments, which is likely to place a higher demand on motor and cognitive resources. Therefore, asking people with MS whether they have problems doing 2 tasks at the same time may provide more accurate information regarding the patients' dual-tasking ability, and subsequently their falls risk, than attempting to objectively measure it.

While patterns of CMI have been examined in other neurological conditions such as stroke and Parkinson disease,22,51 this is the first study to research patterns of CMI and falls status in MS. Previous research examining the effect of dual-task activities in people with MS demonstrated significant deteriorations in gait with an added cognitive task, including altered swing time variability, increased double support time, and a large decrease in gait speed.52,53 Differences between fallers and nonfallers adopting each pattern of CMI in this study were significant for group 6 (changes in gait, numbers correct). This subgroup, along with group 3 (changes in gait and incorrect numbers), was one of the most common patterns utilized by participants and this may suggest that people with MS are not prioritizing the different components of a complex task appropriately similar to what has been observed in people with Parkinson disease.54 This may be a consequence of the limited processing capacity of the brain as highlighted in the attentional capacity theory and the bottleneck theory that have both been used to explain CMI behavior.55 However, these results should be interpreted with caution as there were small numbers in each of the subgroups using each type of pattern and a much larger sample would need to be analyzed to draw any strong conclusions.

There were several strengths to this study including a large sample size, a very low attrition rate, and use of the criterion standard recommendations of a specific falls definition and prospectively recorded falls data38 for a 3-month period. However, the findings from this study should be interpreted with consideration of its limitations. The progressive nature of this study cohort with median Expanded Disability Status Scale score of 6 limits the generalizability of the findings and results may not be applicable in a milder MS cohort. The cognitive task chosen was one of serial subtraction but it has been suggested that verbal fluency tasks may be more appropriate when assessing DTC in MS,56 and the investigators had no knowledge of baseline arithmetic competency levels of the participants. To fully investigate DTC, both the cognitive task and the motor task should be assessed under single- and dual-task conditions,57 but only the motor task was assessed under single-task conditions in this study. Indeed, this seems to be a common issue in MS studies examining DTC, as very few studies to date26,53,58 have actually reported the single-task performance of the cognitive task and examined the DTC of cognition as well as motor function. No instructions were given to participants regarding task prioritization and this study used the TUG as a measure of mobility while other studies measure objective balance control26 or different versions of timed walks.25,40 It has been advised that dual-task assessment needs to be standardized to facilitate comparison of results from different studies that will strengthen the evidence base and allow for clearer recommendations.56,57 Finally, the classifications of pattern of CMI used in this study may be considered a methodological limitation. Because of a lack of previously reported patterns of CMI for people with MS, the 6 patterns of CMI utilized were identified through observing the patterns of the first 12 study participants, but this method may have missed later characteristics that were not observed in that small initial sample.

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CONCLUSION

The findings of this study suggest that objectively measured DTC is not associated with falls status in a more progressive MS cohort who are relatively “young” but presenting with falls at a rate greater than “older” people. The subjective measurement of dual-tasking ability is related to falls status and may be an easy method of screening for falls risk. Simply asking whether they have a problem performing 2 tasks at once is a quick, easy, and cost-free method of establishing dual-tasking ability and may be a useful adjunct in evaluating falls risk. In addition, differences appear to exist between fallers and nonfallers on the basis of whether they prioritize their cognitive or motor task under dual-task conditions. Future research involving more robust analysis and classification of patterns of CMI in a larger sample with a standardized method of DTC assessment will give a clearer insight into the role of DTC and CMI in falls risk assessment and its potential relevance as a component of falls interventions for people with MS.

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Keywords:

accidental falls; cognitive-motor interference; dual-task cost; multiple sclerosis

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