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The Effect of Cognitive Dual Tasks on Balance During Walking in Physically Fit Elderly People
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ORIGINAL ARTICLE
The Effect of Cognitive Dual Tasks on Balance During Walking in Physically Fit Elderly People Marianne B. van Iersel, MD, Heleen Ribbers, MD, Marten Munneke, PhD, George F. Borm, PhD, Marcel G. Olde Rikkert, PhD ABSTRACT. van Iersel MB, Ribbers H, Munneke M, Borm GF, Olde Rikkert MG. The effect of cognitive dual tasks on balance during walking in physically fit elderly people. Arch Phys Med Rehabil 2007;88:187-91. Objective: To evaluate the effect on balance of 3 different cognitive dual tasks performed while walking without and with standardization for gait velocity, and measured with both foot placements and trunk movements. Design: Cross-sectional study. Setting: Community. Participants: Fifty-nine physically fit elderly people (mean age, 73.5y). Interventions: Not applicable. Main Outcome Measures: Stride length and time variability measured with an electronic walkway, body sway measured with an angular velocity instrument, and gait velocity. Results: Overall, dual tasks resulted in decreased gait velocity (1.46 to 1.23m/s, P⬍.001), increased stride length (1.4% to 2.6%), and time variability (1.3% to 2.3%) (P⬍.001), and had no significant effect on body sway. After standardization for gait velocity, the dual tasks were associated with increased body sway (111% to 216% of values during walking without dual task, P⬍.001) and increased stride length and time variability (41% to 223% increase, P⬍.001). Conclusions: In physically fit elderly people, cognitive dual tasks influence balance control during walking directly as well as indirectly through decreased gait velocity. Dual tasks increase stride variability with both mechanisms, but the increase in body sway is only visible after standardization for gait velocity. The decreased gait velocity can be a strategy with which to maintain balance during walking in more difficult circumstances. Key Words: Equilibrium; Gait; Rehabilitation; Task performance and analysis. © 2007 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation ALLS ARE A COMMON PROBLEM among elderly people. Thirty percent of community-living people aged 65 F and over fall at least once a year and that rate increases to 40% among people more than 80 years old. Important risk factors
From the Departments of Geriatrics (van Iersel, Ribbers, Olde Rikkert), Neurology and Physiotherapy (Munneke), and Epidemiology and Biostatistics (Borm), Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Correspondence to Marianne B. van Iersel, MD, Radboud University Nijmegen Medical Centre, Dept of Geriatrics, internal code 925, PO Box 9101, 6500 HB Nijmegen, The Netherlands, e-mail: [email protected]. Reprints are not available from the author. 0003-9993/07/8802-10908$32.00/0 doi:10.1016/j.apmr.2006.10.031
for falls are gait and balance impairments.1 In daily life people often do several other things while they are standing or walking. Many falls occur during the performance of such dual tasks.2 The explanation for this phenomenon is that performing the second task interferes with balance control, probably because of divided attention, or through structural inference in neural networks of the frontal and motor cortex.3,4 A thorough knowledge of the effect of dual tasks on gait and balance may increase our understanding of balance control and can help identify people who are at risk of falling.5,6 Many studies have investigated balance with static measurements, but most falls occur during movement when the center of mass cannot be maintained within the lateral borders of the base of support. Balance during walking is controlled through both foot placements and trunk motion. However, former studies7,8 investigated balance during walking mainly with gait variables such as gait velocity stride width, and stride variability. Some studies4,7,9 involving healthy elderly people found that the addition of a dual task only minimally changed these gait variables. The dual tasks in those studies probably were not sufficiently complex to interfere with balance control. Another possible explanation is that the measurement of balance with only gait variables during walking is insufficiently sensitive to change. Menz et al10 found that adopting a slower gait speed with longer double-support phases did not stabilize the movements of head and trunk in a population of community living elderly people. Also, lowering gait velocity can be a strategy with which to maintain balance control in more difficult circumstances. Gait velocity decreases during performance of a dual task8,11,12 and influences gait and balance variables,13,14 but its contribution to the net effect of dual tasks on balance during walking is unknown. Therefore we investigated the effects of 3 different cognitive dual tasks on balance control during walking in physically fit elderly people, as measured by both foot placements and trunk movements. Furthermore we investigated the effect of the dual tasks on balance control during walking after adjusting for the effect of changed gait velocity on these variables. METHODS Participants We performed a cross-sectional study of physically fit elderly people who had good mobility. All were participants in the international Annual Four-Day Marches Nijmegen, in which elderly hikers walk 30 or 40km a day on 4 consecutive days. We recruited our participants with advertisements in the local and regional newspapers and the leaflet of the Four-Day Marches. Eligible participants were free of any complaints about their gait and balance, were 70 years old or older, had a normal gait pattern as observed by the researchers (MBI, HR), and could perform the Timed Up & Go (TUG) test within 10 seconds.15 All subjects gave their written informed consent to participate. Exclusion criteria were cognitive impairments Arch Phys Med Rehabil Vol 88, February 2007
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EFFECT DUAL TASKS ON BALANCE DURING WALKING, van Iersel Table 1: Population Characteristics (Nⴝ59) Characteristics
Mean ⫾ SD
Men/women (n) Age (y) Length (m) Weight (kg) ISEI⫺9230 Voorrips sport31 CIRS-G32 No. of drugs Subjects who fell in previous year, n (%) Fear of falling (yes/no question), n (%) Visual complaints (n) GARS33 MMSE16* GDS⫺417 (median) UPDRS motor part34 TUG (s)35 Hand grip strength (kg)36
41/18 73.5⫾3.4 (70–82) 1.73⫾0.09 73.7⫾11.2 51.7⫾12.3 (16–87) 12.6⫾4.2 2.9⫾2.1 1.7⫾1.7 14 (24) 9 (15) 3 18.1⫾0.4 28.6⫾1.4 0 0.3⫾0.5 6.2⫾1.0 38.1⫾9.4
NOTE. Values are mean ⫾ standard deviation (SD), mean ⫾ SD (range), or as otherwise indicated. Abbreviations: CIRS-G, Cumulative Illness Rating Scale–Geriatrics (comorbidity index) (scores ⱖ6 indicate frailty); GARS, Groningen Activity Restriction Scale (range, 18 –76, with 18 corresponding to complete independence); ISEI–92, International Socio-Economic Index of occupational status 1992 (range, 16 – 87, with higher score indicating higher status); Voorrips sport, Voorrips sport participation subscale (range 0 –18, with higher score meaning more participation); UPDRS motor part, Unified Parkinson’s Disease Rating Scale motor part. *Range, 0 –30, with scores ⬍25 indicating cognitive impairment.
(Mini-Mental State Examination [MMSE] score, ⬍24/30)16 and depressive symptoms (Geriatric Depression Scale [GDS]⫺4 score, ⱖ3/4).17 Because of a lack of knowledge about balance during walking in the elderly per se, we chose these physically fit elderly people as a reference group for the optimal situation. To fall or not to fall is a dichotomous outcome: this very fit group had a low risk of falls and injuries mainly because they had much reserve in balance. Consequently, in most circumstances a decrease in their balance control would not have impaired their balance enough to increase their risk of falling. We expected, however, that the direction of the effects of the dual tasks on balance during walking would be the same in vigorous and more vulnerable older people. Therefore the results of this study can give a first indication of how balance during walking in more vulnerable older people may be affected by dual tasks and can provide data about the best possible performance. The institutional review board of the Radboud University Nijmegen Medical Centre judged that the study did not need to be approved because of the very low risks and negligible burden for the participants, and because the study involved cognitively intact adults. Table 1 lists the baseline characteristics of all participants. Procedures Quantitative gait analysis was performed with a 5.6⫻0.89-m electronic walkway (GAITRitea) with sensor pads (placed 12.7mm apart) connected to a computer. The electronic walkway has a good concurrent validity compared with a clinical stride analyzer (correlations of .99) and good test-retest reliability with intraclass correlation coefficients of .93 and .94 at preferred and quick gait velocity, respectively.18 Balance was measured with 2 angular velocity transducers (Sway Starb) that Arch Phys Med Rehabil Vol 88, February 2007
measure mediolateral (ML) and anteroposterior (AP) angular velocities at 100Hz. The device was attached as a small box with a belt to the backs of the participants and was connected to the computer with a long wire. The software calculated 90% ranges of angular velocities and angles in ML and AP directions. Primary outcomes of our study were stride variability (stride length, stride time, stride width) and ML body sway because increased stride variability,19 ML displacement, and angular velocity are associated with an increased risk of falling.20 During the measurements, the participants walked on the walkway while wearing low-heeled shoes. To measure steady state walking, the subjects started walking 2m before the walkway and then walked toward a chair positioned 2m behind the walkway. A researcher walked alongside the participants to ensure their safety. To increase the number of steps and precision, all tasks were performed twice and the results were averaged for the statistical analyses. The participants walked first at preferred, slow, quick, and very quick speeds without dual tasks on the walkway. Thereafter they walked at their preferred speed while performing 3 different oral dual tasks: subtracting 7 from 100 and 13 from 100 (attention-demanding tasks) and citing words starting with the letters “K” and “O” (verbal fluency task). Participants practiced all 3 cognitive tasks while standing so as to prevent a learning effect. During the second walk participants began with the number reached last in the subtraction task and were asked to name other words in the verbal fluency task. Tasks that interfere with attention or executive functions most likely will also interfere with balance control. Executive functions include a wide range of functions, of which verbal fluency is an example. We asked participants to indicate which of the cognitive tasks were the most difficult for them individually. Statistical Analysis The baseline gait characteristics of patients were summarized as mean ⫾ standard deviation (SD). We used the coefficient of variation (CV) (SD/mean ⫻ 100%) as the measure of variability for stride time, stride length, and stride width. All body sway and stride variables were first log-transformed to remove skewness (Shapiro-Wilks tests, ⬍.00) and heteroscedastity. We constructed a formula based on linear regression analysis (linear mixed models with the participant as the random effect and the various tasks as the fixed effect) that described how body sway and stride variables varied with gait velocity in each participant during walking without an additional task. The first step in our standardization method was the transformation of the gait and balance data to obtain a normal distribution and to decrease the influence of outliers. We then constructed a formula based on regression analysis that described how these data varied with gait velocity in each participant during walking without an additional task. We used this formula to standardize the gait and balance data for the effect of gait velocity for each participant. Thereafter body sway and stride variables stayed the same over the entire range of gait velocities: the influence of gait velocity was removed. We used these results to standardize the variables such that the means without dual task were 100, independent of gait velocity.21 We compared the nonstandardized and standardized results for the dual tasks with the results without dual tasks. We performed an omnibus test (likelihood ratio test) that compared all tasks simultaneously and if this test was significant, the result of each dual task was compared with no task. Likelihood ratio tests were used throughout and the significance level was set at .01 (2-sided) to adjust for multiplicity. To estimate the sample size needed for this study, we made the following assumptions based on duplo-measurements of
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Table 2: Gait and Balance Variables During Walking at 4 Different Gait Velocities Without Dual Tasking in Physically Fit Elderly People Gait Velocity Balance and Gait Variables
Slow
Preferred
Quick
Very Quick
P (omnibus test)
Displacement ML (deg) Angular velocity ML (deg/s) Displacement AP (deg) Angular velocity AP (deg/s) Gait velocity (m/s) Cadence (steps/min) Stride length (cm) Stride width (cm) Stride length variability (%CV) Stride time variability (%CV) Stride width variability (%CV)
3.8⫾1.3* 30.7⫾1.3* 5.6⫾1.3* 37.2⫾1.4* 1.03⫾0.18* 97.1⫾9.7* 127.3⫾14.5* 10.1⫾2.9 2.0⫾63.1* 1.8⫾57.2* 15.6⫾48.5
4.5⫾1.4 42.8⫾1.4 8.4⫾1.3 63.0⫾1.5 1.46⫾0.18 117.6⫾7.6 150.1⫾16.4 10.0⫾2.9 1.4⫾61.7 1.3⫾62.3 15.4⫾88.5
5.5⫾1.5* 52.7⫾1.4* 10.0⫾1.3* 82.8⫾1.5* 1.63⫾0.24* 126.3⫾10.0* 155.7⫾17.1* 9.7⫾3.0 1.6⫾61.4 1.2⫾66.6 14.2⫾79.5
6.7⫾1.4* 72.9⫾1.4* 13.2⫾1.3* 124.7⫾1.5* 2.00⫾0.19* 146.5⫾16.8* 165.3⫾19.1* 9.6⫾3.1 1.8⫾106.6 1.3⫾65.0 17.6⫾83.1
⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001
NOTE. Values are mean ⫾ SD. All means are back transformed from the log-transformed values except gait velocity, cadence, stride length, and stride width. Data were tested for difference versus reference condition (walking at preferred gait velocity). *P⬍.001.
gait velocity from a pilot study: to detect a difference of .10m/s in gait velocity with a power of 90% and a significance level of .05, a total sample size of 58 patients was needed. All data were analyzed using SPSSc statistical software. RESULTS Of the 62 people recruited, we included 59 (mean age ⫾ SD, 73.5⫾3.5y), of whom 18 were women (see table 1). One person was excluded because of an MMSE score of 23 and 1 because of a GDS score of 3. Because of a technical problem in the Sway Star a high percentage of data was missing for a third person who also was excluded. The participants were active and physically highly fit elderly people with a large range in their socioeconomic status. During walking without dual tasks, an increase in gait velocity resulted in increases in angular displacement and velocity in both directions. Variability of stride length, time, and stride width increased if gait velocity decreased and increased from the reference condition (walking at preferred gait velocity) (table 2). Table 3 shows the values of the gait and balance variables during the different dual-task conditions. Body sway did not change significantly after the dual tasks were added. Variability in stride width also stayed the same during all
conditions. Variability in stride length and stride time increased from 1.4% and 1.3% during walking without dual tasks to 2.6% and 2.3%, respectively, with the verbal fluency task (P⬍.01). The spread in all variability measures was large. Gait velocity decreased from 1.46m/s without a dual task to 1.34m/s during the execution of the 100 minus 13 task and to 1.23m/s during the verbal fluency dual task (P⬍.01). After standardization of body sway and stride variability for gait velocity, the effects of dual tasks on body sway and stride variability were equivocal: they all pointed toward more body sway and increased stride variability except that there was no change in stride width variability (table 4). Subtracting 7 from 100 had the fewest effects on body sway and stride variability and the verbal fluency task had the largest effect. DISCUSSION This study shows that performance of dual tasks while walking influences balance in physically fit elderly people through a direct effect on body sway and stride variability and an indirect effect through gait velocity. Dual tasks decrease gait velocity, which in itself is associated with a decrease in body sway and an increase in stride variability. After standardization for gait velocity, both body sway and stride variability in-
Table 3: Gait and Balance at Preferred Gait Velocity With and Without Dual Tasking (Reference Condition) Walking at Preferred Gait Velocity Cognitive Dual Tasks Balance and Gait Variables
Reference No Dual Task
100–7
100–13
K and O
P (omnibus test)
Displacement ML (deg) Angular velocity ML (deg/s) Displacement AP (deg) Angular velocity AP (deg/s) Gait velocity (m/s) Cadence (steps/min) Stride length (cm) Stride width (cm) Stride length variability (%CV) Stride time variability (%CV) Stride width variability (%CV)
4.6⫾1.4 42.7⫾1.4 8.4⫾1.3 63.0⫾1.5 1.46⫾0.18 118⫾7.6 150.0⫾16.4 10.0⫾2.9 1.4⫾0.6 1.3⫾0.6 15.4⫾0.9
4.8⫾1.4 45.1⫾1.4 8.3⫾1.4 65.2⫾1.6 1.41⫾0.24 114⫾12.0 147.4⫾18.3 10.0⫾3.1 1.8⫾0.6 1.6⫾0.6 15.4⫾0.6
4.6⫾1.6 42.4⫾1.4 8.3⫾1.4 62.4⫾1.6 1.34⫾0.26 110⫾15.5 145.4⫾19.6 10.3⫾3.3 2.2⫾0.7 2.0⫾1.0 18.5⫾0.6
4.5⫾1.4 40.6⫾1.4 7.4⫾1.4 58.3⫾1.5 1.23⫾0.26* 105⫾16.9 141.5⫾19.3 10.7⫾2.9 2.6⫾0.7* 2.3⫾1.1* 16.5⫾0.6
.905 .008 .060 .014 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001
NOTE. Values are mean ⫾ SD. Data were tested for difference versus reference condition. All means are back-transformed from the log-transformed values except gait velocity, cadence, stride length, and stride width. *P⬍.01.
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Table 4: Comparison of Relative Values of Body Sway and Stride Variability, Standardized for Gait Velocity, While Walking With a Dual Task Versus Walking Without a Dual Task (reference condition, 100) Walking Without and With 3 Different Cognitive Dual Tasks Cognitive Dual Tasks Balance and Gait Variables
Reference No Dual Task
100–7
100⫾37 100⫾36 100⫾41 100⫾55 100⫾54 100⫾45 100⫾58
122⫾60 110⫾37† 123⫾62 127⫾70* 107⫾45 145⫾64* 99⫾53
Displacement ML Angular velocity ML Displacement AP Angular velocity AP Stride length variability Stride time variability Stride width variability
100–13
133⫾66† 110⫾34† 168⫾140† 164⫾121† 175⫾152† 275⫾323† 116⫾66
K and O
P (omnibus test)
16⫾127* 116⫾34† 243⫾294† 237⫾259† 141⫾84† 323⫾360† 105⫾56
⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 .46
NOTE. Values are mean ⫾ SD. Data were tested for difference versus reference condition. *P⬍.01; †P⬍.001.
creased during dual-task performance. The slowing of gait while performing a dual task may reflect a purposeful adaptation to reduce the risk of falls in more difficult circumstances and can be seen in several patient categories.10-12,22 This could be a reason why in some studies4,7,9 dual tasks did not change foot placements. We found, however, significant changes in stride length and stride time variability for all dual-task conditions without standardization for gait velocity. In contrast, the dual tasks did not have a significant effect on stride width variability. This is in line with the findings of Hausdorff et al,23 but is the opposite of Maki’s19 results. Grabiner and Troy24 described a decrease in step width variability when a dual task was added. Although they do not provide a full explanation, probable reasons for these conflicting results are: the difference in treadmill and over ground walking, a dual task with visual input that requires focusing on a point ahead compared with verbal input, the effect of dual tasks on both gait velocity and stride width variability, and different units of measurement for variability (SDs vs CVs). To our knowledge, the only study that tested the effect of a dual task on balance during walking measured with body sway is that of de Hoon et al.2 They showed that elderly people who fall had more body sway during walking than did nonfallers. Their results are difficult to compare with our results, however, because they used a single question as a dual task to test the balance reaction to an unexpected situation and did not use division of attention or structural inference during performance of a continuous dual task. They did not correct their findings for variation in gait velocity among the participants; also, our population was much more vigorous. More is known about the effect of attention and executive functions on gait and balance. They appear to be the most important cognitive functions in the regulation of gait and balance control in older people. This is shown in direct associations of cognitive functioning with gait velocity and falls.25,26 Other studies27,28 provide evidence of the usefulness of dual tasks in investigations of the risks of falling in elderly people. Springer et al22 showed that dual tasks influence swing time variability in older fallers but not in young people or older nonfallers, and that this response correlated significantly with executive function. This information can be used as background for interpreting the clinical relevance of the current findings. Our participants perceived the verbal fluency task as the most difficult of the cognitive tasks and subtracting 7 from 100 as the easiest. They made more mistakes while subtracting 13 from 100 than while subtracting 7 from 100, and they could count less far back. The result of citing words starting with a K and O ranged from no good words to 5 per trial. Arch Phys Med Rehabil Vol 88, February 2007
Study Limitations An important limitation of this study is that the clinical relevance of dual tasks in balance during walking measurements still must be proved. Our participants were physically very highly fit29 and had only a small risk of falling. Therefore we cannot infer from the results of this study the combinations of tests that are most useful for identifying fallers. In a post hoc analysis, participants who reported a fall did not show differences in gait and balance results when compared with nonfallers. The number of fallers was very small, however, so it is likely that we did not have enough power to detect differences between the 2 groups. As we explained in the Methods section, we expected that the direction of the effect of the dual tasks on gait and balance variables would be the same in both vigorous and vulnerable older people. Whether this is coupled with an increased risk of falling depends on the basic level of balance control. Therefore we can say something about the mechanism itself in an optimal situation, but we cannot infer from our results the people who have an increased risk of falling. To our knowledge we are the first to investigate the effect of cognitive dual tasks on balance during walking, measured with both foot placements and trunk movements, and taking into consideration the effect of the dual tasks on gait velocity. Although we selected the most important outcome variables before the study, it was an explorative study with many comparisons and this is a limitation of it. There are 2 other limitations. One, the number of steps in each walk was limited because of the relatively short length of the walkway. This may have reduced the precision of the measurements. Second, the amount of attention given to the cognitive task can influence the effect of the task on gait and balance. Because our primary goal was to investigate the effect of cognitive dual tasks on balance during walking, we did not score the subjects’ performances on the attention and verbal fluency tasks while standing still. Therefore we cannot calculate the cost of walking on the dual task. CONCLUSIONS This study provides more insight into the interaction of dual tasks with balance control during walking in physically fit elderly people. It emphasizes the importance of investigating balance during walking with both foot placements and body sway and with and without standardization for gait velocity. Prospective studies are needed to investigate the reliability and responsiveness of these balance measures and to test their usefulness in evaluating the effect of interventions on gait, balance, and risk of falling in more frail elderly patients.
EFFECT DUAL TASKS ON BALANCE DURING WALKING, van Iersel
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21. van Iersel MB, Olde Rikkert MG, Borm GF. A method to standardize gait and balance variables for gait velocity. Gait Posture. In press. 22. Springer S, Giladi N, Peretz C, Yogev G, Simon ES, Hausdorff JM. Dual-tasking effects on gait variability: the role of aging, falls, and executive function. Mov Disord 2006;21:950-7. 23. Hausdorff JM, Rios DA, Edelberg HK. Gait variability and fall risk in community-living older adults: a 1-year prospective study. Arch Phys Med Rehabil 2001;82:1050-6. 24. Grabiner MD, Troy KL. Attention demanding tasks during treadmill walking reduce step width variability in young adults. J Neuroengineering Rehabil 2005;2:25. 25. Ble A, Volpato S, Zuliani G, et al. Executive function correlates with walking speed in older persons: the InCHIANTI study. J Am Geriatr Soc 2005;53:410-5. 26. Holtzer R, Verghese J, Xue X, Lipton RB. Cognitive processes related to gait velocity: results from the Einstein Aging Study. Neuropsychology 2006;20:215-23. 27. Bootsma-van der Wiel A, Gussekloo J, De Craen AJ, Van Exel E, Bloem BR, Westendorp RG. Walking and talking as predictors of falls in the general population: the Leiden 85-Plus Study. J Am Geriatr Soc 2003;51:1466-71. 28. Verghese J, Buschke H, Viola L, et al. Validity of divided attention tasks in predicting falls in older individuals: a preliminary study. J Am Geriatr Soc 2002;50:1572-6. 29. de Wild GM, Hoefnagels WH, Oeseburg B, Binkhorst RA. Maximal oxygen uptake in 153 elderly Dutch people (69-87 years) who participated in the 1993 Nijmegen 4-day march. Eur J Appl Physiol Occup Physiol 1995;72:134-43. 30. Bakker B, Sieben I, Nieuwbeerta P, Ganzeboom H. [Scales for prestige, socio-economic status and social class for the Standard Occupational Classification 1992] [Dutch]. Soc Wetenschappen 1997;40:1-22. 31. Voorrips LE, Ravelli AC, Dongelmans PC, Deurenberg P, van Staveren WA. A physical activity questionnaire for the elderly. Med Sci Sports Exerc 1991;23:974-9. 32. Parmelee PA, Thuras PD, Katz IR, Lawton MP. Validation of the Cumulative Illness Rating Scale in a geriatric residential population. J Am Geriatr Soc 1995;43:130-7. 33. Suurmeijer TP, Doeglas DM, Moum T, et al. The Groningen Activity Restriction Scale for measuring disability: its utility in international comparisons. Am J Public Health 1994;84:1270-3. 34. Martinez-Martin P, Gil-Nagel A, Gracia LM, Gomez JB, Martinez-Sarries J, Bermejo F. Unified Parkinson’s Disease Rating Scale characteristics and structure. The Cooperative Multicentric Group. Mov Disord 1994;9:76-83. 35. Podsiadlo D, Richardson S. The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 1991;39:142-8. 36. Syddall H, Cooper C, Martin F, Briggs R, Aihie SA. Is grip strength a useful single marker of frailty? Age Ageing 2003;32: 650-6. Suppliers a. CIR Systems Inc, 60 Garlor Dr, Havertown, PA 19083. b. Balance International Innovations GmbH, PO Box 11, CH-3807, Iseltwald, Switzerland. c. Version 12.0; SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.
Arch Phys Med Rehabil Vol 88, February 2007
ORIGINAL ARTICLE
The Effect of Cognitive Dual Tasks on Balance During Walking in Physically Fit Elderly People Marianne B. van Iersel, MD, Heleen Ribbers, MD, Marten Munneke, PhD, George F. Borm, PhD, Marcel G. Olde Rikkert, PhD ABSTRACT. van Iersel MB, Ribbers H, Munneke M, Borm GF, Olde Rikkert MG. The effect of cognitive dual tasks on balance during walking in physically fit elderly people. Arch Phys Med Rehabil 2007;88:187-91. Objective: To evaluate the effect on balance of 3 different cognitive dual tasks performed while walking without and with standardization for gait velocity, and measured with both foot placements and trunk movements. Design: Cross-sectional study. Setting: Community. Participants: Fifty-nine physically fit elderly people (mean age, 73.5y). Interventions: Not applicable. Main Outcome Measures: Stride length and time variability measured with an electronic walkway, body sway measured with an angular velocity instrument, and gait velocity. Results: Overall, dual tasks resulted in decreased gait velocity (1.46 to 1.23m/s, P⬍.001), increased stride length (1.4% to 2.6%), and time variability (1.3% to 2.3%) (P⬍.001), and had no significant effect on body sway. After standardization for gait velocity, the dual tasks were associated with increased body sway (111% to 216% of values during walking without dual task, P⬍.001) and increased stride length and time variability (41% to 223% increase, P⬍.001). Conclusions: In physically fit elderly people, cognitive dual tasks influence balance control during walking directly as well as indirectly through decreased gait velocity. Dual tasks increase stride variability with both mechanisms, but the increase in body sway is only visible after standardization for gait velocity. The decreased gait velocity can be a strategy with which to maintain balance during walking in more difficult circumstances. Key Words: Equilibrium; Gait; Rehabilitation; Task performance and analysis. © 2007 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation ALLS ARE A COMMON PROBLEM among elderly people. Thirty percent of community-living people aged 65 F and over fall at least once a year and that rate increases to 40% among people more than 80 years old. Important risk factors
From the Departments of Geriatrics (van Iersel, Ribbers, Olde Rikkert), Neurology and Physiotherapy (Munneke), and Epidemiology and Biostatistics (Borm), Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Correspondence to Marianne B. van Iersel, MD, Radboud University Nijmegen Medical Centre, Dept of Geriatrics, internal code 925, PO Box 9101, 6500 HB Nijmegen, The Netherlands, e-mail: [email protected]. Reprints are not available from the author. 0003-9993/07/8802-10908$32.00/0 doi:10.1016/j.apmr.2006.10.031
for falls are gait and balance impairments.1 In daily life people often do several other things while they are standing or walking. Many falls occur during the performance of such dual tasks.2 The explanation for this phenomenon is that performing the second task interferes with balance control, probably because of divided attention, or through structural inference in neural networks of the frontal and motor cortex.3,4 A thorough knowledge of the effect of dual tasks on gait and balance may increase our understanding of balance control and can help identify people who are at risk of falling.5,6 Many studies have investigated balance with static measurements, but most falls occur during movement when the center of mass cannot be maintained within the lateral borders of the base of support. Balance during walking is controlled through both foot placements and trunk motion. However, former studies7,8 investigated balance during walking mainly with gait variables such as gait velocity stride width, and stride variability. Some studies4,7,9 involving healthy elderly people found that the addition of a dual task only minimally changed these gait variables. The dual tasks in those studies probably were not sufficiently complex to interfere with balance control. Another possible explanation is that the measurement of balance with only gait variables during walking is insufficiently sensitive to change. Menz et al10 found that adopting a slower gait speed with longer double-support phases did not stabilize the movements of head and trunk in a population of community living elderly people. Also, lowering gait velocity can be a strategy with which to maintain balance control in more difficult circumstances. Gait velocity decreases during performance of a dual task8,11,12 and influences gait and balance variables,13,14 but its contribution to the net effect of dual tasks on balance during walking is unknown. Therefore we investigated the effects of 3 different cognitive dual tasks on balance control during walking in physically fit elderly people, as measured by both foot placements and trunk movements. Furthermore we investigated the effect of the dual tasks on balance control during walking after adjusting for the effect of changed gait velocity on these variables. METHODS Participants We performed a cross-sectional study of physically fit elderly people who had good mobility. All were participants in the international Annual Four-Day Marches Nijmegen, in which elderly hikers walk 30 or 40km a day on 4 consecutive days. We recruited our participants with advertisements in the local and regional newspapers and the leaflet of the Four-Day Marches. Eligible participants were free of any complaints about their gait and balance, were 70 years old or older, had a normal gait pattern as observed by the researchers (MBI, HR), and could perform the Timed Up & Go (TUG) test within 10 seconds.15 All subjects gave their written informed consent to participate. Exclusion criteria were cognitive impairments Arch Phys Med Rehabil Vol 88, February 2007
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EFFECT DUAL TASKS ON BALANCE DURING WALKING, van Iersel Table 1: Population Characteristics (Nⴝ59) Characteristics
Mean ⫾ SD
Men/women (n) Age (y) Length (m) Weight (kg) ISEI⫺9230 Voorrips sport31 CIRS-G32 No. of drugs Subjects who fell in previous year, n (%) Fear of falling (yes/no question), n (%) Visual complaints (n) GARS33 MMSE16* GDS⫺417 (median) UPDRS motor part34 TUG (s)35 Hand grip strength (kg)36
41/18 73.5⫾3.4 (70–82) 1.73⫾0.09 73.7⫾11.2 51.7⫾12.3 (16–87) 12.6⫾4.2 2.9⫾2.1 1.7⫾1.7 14 (24) 9 (15) 3 18.1⫾0.4 28.6⫾1.4 0 0.3⫾0.5 6.2⫾1.0 38.1⫾9.4
NOTE. Values are mean ⫾ standard deviation (SD), mean ⫾ SD (range), or as otherwise indicated. Abbreviations: CIRS-G, Cumulative Illness Rating Scale–Geriatrics (comorbidity index) (scores ⱖ6 indicate frailty); GARS, Groningen Activity Restriction Scale (range, 18 –76, with 18 corresponding to complete independence); ISEI–92, International Socio-Economic Index of occupational status 1992 (range, 16 – 87, with higher score indicating higher status); Voorrips sport, Voorrips sport participation subscale (range 0 –18, with higher score meaning more participation); UPDRS motor part, Unified Parkinson’s Disease Rating Scale motor part. *Range, 0 –30, with scores ⬍25 indicating cognitive impairment.
(Mini-Mental State Examination [MMSE] score, ⬍24/30)16 and depressive symptoms (Geriatric Depression Scale [GDS]⫺4 score, ⱖ3/4).17 Because of a lack of knowledge about balance during walking in the elderly per se, we chose these physically fit elderly people as a reference group for the optimal situation. To fall or not to fall is a dichotomous outcome: this very fit group had a low risk of falls and injuries mainly because they had much reserve in balance. Consequently, in most circumstances a decrease in their balance control would not have impaired their balance enough to increase their risk of falling. We expected, however, that the direction of the effects of the dual tasks on balance during walking would be the same in vigorous and more vulnerable older people. Therefore the results of this study can give a first indication of how balance during walking in more vulnerable older people may be affected by dual tasks and can provide data about the best possible performance. The institutional review board of the Radboud University Nijmegen Medical Centre judged that the study did not need to be approved because of the very low risks and negligible burden for the participants, and because the study involved cognitively intact adults. Table 1 lists the baseline characteristics of all participants. Procedures Quantitative gait analysis was performed with a 5.6⫻0.89-m electronic walkway (GAITRitea) with sensor pads (placed 12.7mm apart) connected to a computer. The electronic walkway has a good concurrent validity compared with a clinical stride analyzer (correlations of .99) and good test-retest reliability with intraclass correlation coefficients of .93 and .94 at preferred and quick gait velocity, respectively.18 Balance was measured with 2 angular velocity transducers (Sway Starb) that Arch Phys Med Rehabil Vol 88, February 2007
measure mediolateral (ML) and anteroposterior (AP) angular velocities at 100Hz. The device was attached as a small box with a belt to the backs of the participants and was connected to the computer with a long wire. The software calculated 90% ranges of angular velocities and angles in ML and AP directions. Primary outcomes of our study were stride variability (stride length, stride time, stride width) and ML body sway because increased stride variability,19 ML displacement, and angular velocity are associated with an increased risk of falling.20 During the measurements, the participants walked on the walkway while wearing low-heeled shoes. To measure steady state walking, the subjects started walking 2m before the walkway and then walked toward a chair positioned 2m behind the walkway. A researcher walked alongside the participants to ensure their safety. To increase the number of steps and precision, all tasks were performed twice and the results were averaged for the statistical analyses. The participants walked first at preferred, slow, quick, and very quick speeds without dual tasks on the walkway. Thereafter they walked at their preferred speed while performing 3 different oral dual tasks: subtracting 7 from 100 and 13 from 100 (attention-demanding tasks) and citing words starting with the letters “K” and “O” (verbal fluency task). Participants practiced all 3 cognitive tasks while standing so as to prevent a learning effect. During the second walk participants began with the number reached last in the subtraction task and were asked to name other words in the verbal fluency task. Tasks that interfere with attention or executive functions most likely will also interfere with balance control. Executive functions include a wide range of functions, of which verbal fluency is an example. We asked participants to indicate which of the cognitive tasks were the most difficult for them individually. Statistical Analysis The baseline gait characteristics of patients were summarized as mean ⫾ standard deviation (SD). We used the coefficient of variation (CV) (SD/mean ⫻ 100%) as the measure of variability for stride time, stride length, and stride width. All body sway and stride variables were first log-transformed to remove skewness (Shapiro-Wilks tests, ⬍.00) and heteroscedastity. We constructed a formula based on linear regression analysis (linear mixed models with the participant as the random effect and the various tasks as the fixed effect) that described how body sway and stride variables varied with gait velocity in each participant during walking without an additional task. The first step in our standardization method was the transformation of the gait and balance data to obtain a normal distribution and to decrease the influence of outliers. We then constructed a formula based on regression analysis that described how these data varied with gait velocity in each participant during walking without an additional task. We used this formula to standardize the gait and balance data for the effect of gait velocity for each participant. Thereafter body sway and stride variables stayed the same over the entire range of gait velocities: the influence of gait velocity was removed. We used these results to standardize the variables such that the means without dual task were 100, independent of gait velocity.21 We compared the nonstandardized and standardized results for the dual tasks with the results without dual tasks. We performed an omnibus test (likelihood ratio test) that compared all tasks simultaneously and if this test was significant, the result of each dual task was compared with no task. Likelihood ratio tests were used throughout and the significance level was set at .01 (2-sided) to adjust for multiplicity. To estimate the sample size needed for this study, we made the following assumptions based on duplo-measurements of
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Table 2: Gait and Balance Variables During Walking at 4 Different Gait Velocities Without Dual Tasking in Physically Fit Elderly People Gait Velocity Balance and Gait Variables
Slow
Preferred
Quick
Very Quick
P (omnibus test)
Displacement ML (deg) Angular velocity ML (deg/s) Displacement AP (deg) Angular velocity AP (deg/s) Gait velocity (m/s) Cadence (steps/min) Stride length (cm) Stride width (cm) Stride length variability (%CV) Stride time variability (%CV) Stride width variability (%CV)
3.8⫾1.3* 30.7⫾1.3* 5.6⫾1.3* 37.2⫾1.4* 1.03⫾0.18* 97.1⫾9.7* 127.3⫾14.5* 10.1⫾2.9 2.0⫾63.1* 1.8⫾57.2* 15.6⫾48.5
4.5⫾1.4 42.8⫾1.4 8.4⫾1.3 63.0⫾1.5 1.46⫾0.18 117.6⫾7.6 150.1⫾16.4 10.0⫾2.9 1.4⫾61.7 1.3⫾62.3 15.4⫾88.5
5.5⫾1.5* 52.7⫾1.4* 10.0⫾1.3* 82.8⫾1.5* 1.63⫾0.24* 126.3⫾10.0* 155.7⫾17.1* 9.7⫾3.0 1.6⫾61.4 1.2⫾66.6 14.2⫾79.5
6.7⫾1.4* 72.9⫾1.4* 13.2⫾1.3* 124.7⫾1.5* 2.00⫾0.19* 146.5⫾16.8* 165.3⫾19.1* 9.6⫾3.1 1.8⫾106.6 1.3⫾65.0 17.6⫾83.1
⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001
NOTE. Values are mean ⫾ SD. All means are back transformed from the log-transformed values except gait velocity, cadence, stride length, and stride width. Data were tested for difference versus reference condition (walking at preferred gait velocity). *P⬍.001.
gait velocity from a pilot study: to detect a difference of .10m/s in gait velocity with a power of 90% and a significance level of .05, a total sample size of 58 patients was needed. All data were analyzed using SPSSc statistical software. RESULTS Of the 62 people recruited, we included 59 (mean age ⫾ SD, 73.5⫾3.5y), of whom 18 were women (see table 1). One person was excluded because of an MMSE score of 23 and 1 because of a GDS score of 3. Because of a technical problem in the Sway Star a high percentage of data was missing for a third person who also was excluded. The participants were active and physically highly fit elderly people with a large range in their socioeconomic status. During walking without dual tasks, an increase in gait velocity resulted in increases in angular displacement and velocity in both directions. Variability of stride length, time, and stride width increased if gait velocity decreased and increased from the reference condition (walking at preferred gait velocity) (table 2). Table 3 shows the values of the gait and balance variables during the different dual-task conditions. Body sway did not change significantly after the dual tasks were added. Variability in stride width also stayed the same during all
conditions. Variability in stride length and stride time increased from 1.4% and 1.3% during walking without dual tasks to 2.6% and 2.3%, respectively, with the verbal fluency task (P⬍.01). The spread in all variability measures was large. Gait velocity decreased from 1.46m/s without a dual task to 1.34m/s during the execution of the 100 minus 13 task and to 1.23m/s during the verbal fluency dual task (P⬍.01). After standardization of body sway and stride variability for gait velocity, the effects of dual tasks on body sway and stride variability were equivocal: they all pointed toward more body sway and increased stride variability except that there was no change in stride width variability (table 4). Subtracting 7 from 100 had the fewest effects on body sway and stride variability and the verbal fluency task had the largest effect. DISCUSSION This study shows that performance of dual tasks while walking influences balance in physically fit elderly people through a direct effect on body sway and stride variability and an indirect effect through gait velocity. Dual tasks decrease gait velocity, which in itself is associated with a decrease in body sway and an increase in stride variability. After standardization for gait velocity, both body sway and stride variability in-
Table 3: Gait and Balance at Preferred Gait Velocity With and Without Dual Tasking (Reference Condition) Walking at Preferred Gait Velocity Cognitive Dual Tasks Balance and Gait Variables
Reference No Dual Task
100–7
100–13
K and O
P (omnibus test)
Displacement ML (deg) Angular velocity ML (deg/s) Displacement AP (deg) Angular velocity AP (deg/s) Gait velocity (m/s) Cadence (steps/min) Stride length (cm) Stride width (cm) Stride length variability (%CV) Stride time variability (%CV) Stride width variability (%CV)
4.6⫾1.4 42.7⫾1.4 8.4⫾1.3 63.0⫾1.5 1.46⫾0.18 118⫾7.6 150.0⫾16.4 10.0⫾2.9 1.4⫾0.6 1.3⫾0.6 15.4⫾0.9
4.8⫾1.4 45.1⫾1.4 8.3⫾1.4 65.2⫾1.6 1.41⫾0.24 114⫾12.0 147.4⫾18.3 10.0⫾3.1 1.8⫾0.6 1.6⫾0.6 15.4⫾0.6
4.6⫾1.6 42.4⫾1.4 8.3⫾1.4 62.4⫾1.6 1.34⫾0.26 110⫾15.5 145.4⫾19.6 10.3⫾3.3 2.2⫾0.7 2.0⫾1.0 18.5⫾0.6
4.5⫾1.4 40.6⫾1.4 7.4⫾1.4 58.3⫾1.5 1.23⫾0.26* 105⫾16.9 141.5⫾19.3 10.7⫾2.9 2.6⫾0.7* 2.3⫾1.1* 16.5⫾0.6
.905 .008 .060 .014 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001
NOTE. Values are mean ⫾ SD. Data were tested for difference versus reference condition. All means are back-transformed from the log-transformed values except gait velocity, cadence, stride length, and stride width. *P⬍.01.
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Table 4: Comparison of Relative Values of Body Sway and Stride Variability, Standardized for Gait Velocity, While Walking With a Dual Task Versus Walking Without a Dual Task (reference condition, 100) Walking Without and With 3 Different Cognitive Dual Tasks Cognitive Dual Tasks Balance and Gait Variables
Reference No Dual Task
100–7
100⫾37 100⫾36 100⫾41 100⫾55 100⫾54 100⫾45 100⫾58
122⫾60 110⫾37† 123⫾62 127⫾70* 107⫾45 145⫾64* 99⫾53
Displacement ML Angular velocity ML Displacement AP Angular velocity AP Stride length variability Stride time variability Stride width variability
100–13
133⫾66† 110⫾34† 168⫾140† 164⫾121† 175⫾152† 275⫾323† 116⫾66
K and O
P (omnibus test)
16⫾127* 116⫾34† 243⫾294† 237⫾259† 141⫾84† 323⫾360† 105⫾56
⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 ⬍.001 .46
NOTE. Values are mean ⫾ SD. Data were tested for difference versus reference condition. *P⬍.01; †P⬍.001.
creased during dual-task performance. The slowing of gait while performing a dual task may reflect a purposeful adaptation to reduce the risk of falls in more difficult circumstances and can be seen in several patient categories.10-12,22 This could be a reason why in some studies4,7,9 dual tasks did not change foot placements. We found, however, significant changes in stride length and stride time variability for all dual-task conditions without standardization for gait velocity. In contrast, the dual tasks did not have a significant effect on stride width variability. This is in line with the findings of Hausdorff et al,23 but is the opposite of Maki’s19 results. Grabiner and Troy24 described a decrease in step width variability when a dual task was added. Although they do not provide a full explanation, probable reasons for these conflicting results are: the difference in treadmill and over ground walking, a dual task with visual input that requires focusing on a point ahead compared with verbal input, the effect of dual tasks on both gait velocity and stride width variability, and different units of measurement for variability (SDs vs CVs). To our knowledge, the only study that tested the effect of a dual task on balance during walking measured with body sway is that of de Hoon et al.2 They showed that elderly people who fall had more body sway during walking than did nonfallers. Their results are difficult to compare with our results, however, because they used a single question as a dual task to test the balance reaction to an unexpected situation and did not use division of attention or structural inference during performance of a continuous dual task. They did not correct their findings for variation in gait velocity among the participants; also, our population was much more vigorous. More is known about the effect of attention and executive functions on gait and balance. They appear to be the most important cognitive functions in the regulation of gait and balance control in older people. This is shown in direct associations of cognitive functioning with gait velocity and falls.25,26 Other studies27,28 provide evidence of the usefulness of dual tasks in investigations of the risks of falling in elderly people. Springer et al22 showed that dual tasks influence swing time variability in older fallers but not in young people or older nonfallers, and that this response correlated significantly with executive function. This information can be used as background for interpreting the clinical relevance of the current findings. Our participants perceived the verbal fluency task as the most difficult of the cognitive tasks and subtracting 7 from 100 as the easiest. They made more mistakes while subtracting 13 from 100 than while subtracting 7 from 100, and they could count less far back. The result of citing words starting with a K and O ranged from no good words to 5 per trial. Arch Phys Med Rehabil Vol 88, February 2007
Study Limitations An important limitation of this study is that the clinical relevance of dual tasks in balance during walking measurements still must be proved. Our participants were physically very highly fit29 and had only a small risk of falling. Therefore we cannot infer from the results of this study the combinations of tests that are most useful for identifying fallers. In a post hoc analysis, participants who reported a fall did not show differences in gait and balance results when compared with nonfallers. The number of fallers was very small, however, so it is likely that we did not have enough power to detect differences between the 2 groups. As we explained in the Methods section, we expected that the direction of the effect of the dual tasks on gait and balance variables would be the same in both vigorous and vulnerable older people. Whether this is coupled with an increased risk of falling depends on the basic level of balance control. Therefore we can say something about the mechanism itself in an optimal situation, but we cannot infer from our results the people who have an increased risk of falling. To our knowledge we are the first to investigate the effect of cognitive dual tasks on balance during walking, measured with both foot placements and trunk movements, and taking into consideration the effect of the dual tasks on gait velocity. Although we selected the most important outcome variables before the study, it was an explorative study with many comparisons and this is a limitation of it. There are 2 other limitations. One, the number of steps in each walk was limited because of the relatively short length of the walkway. This may have reduced the precision of the measurements. Second, the amount of attention given to the cognitive task can influence the effect of the task on gait and balance. Because our primary goal was to investigate the effect of cognitive dual tasks on balance during walking, we did not score the subjects’ performances on the attention and verbal fluency tasks while standing still. Therefore we cannot calculate the cost of walking on the dual task. CONCLUSIONS This study provides more insight into the interaction of dual tasks with balance control during walking in physically fit elderly people. It emphasizes the importance of investigating balance during walking with both foot placements and body sway and with and without standardization for gait velocity. Prospective studies are needed to investigate the reliability and responsiveness of these balance measures and to test their usefulness in evaluating the effect of interventions on gait, balance, and risk of falling in more frail elderly patients.
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Arch Phys Med Rehabil Vol 88, February 2007