The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 62:837-843 (2007)
© 2007 The Gerontological Society of America
Impaired Attention Predicts Motor Performance Decline in Older Community-Dwellers With Normal Baseline Mobility: Results From the Italian Longitudinal Study on Aging (ILSA)
Marco Inzitari,
Marzia Baldereschi,
Antonio Di Carlo,
Mauro Di Bari,
Niccolò Marchionni,
Emanuele Scafato,
Gino Farchi,
Domenico Inzitari and
for the ILSA Working Group
1 Department of Critical Care Medicine and Surgery, Unit of Gerontology and Geriatrics, Azienda Ospedaliero-Universitaria Careggi, Florence, Italy.
2 Neuroscience, Italian National Research Council, Pisa, Italy.
3 Laboratorio di Epidemiologia e Biostatistica, Istituto Superiore di Sanità, Rome, Italy.
4 Department of Neurological-Psychiatric Sciences, Azienda Ospedaliero-Universitaria Careggi, Florence, Italy.
Address correspondence to Marco Inzitari, MD, Department of Critical Care Medicine and Surgery, Unit of Gerontology and Geriatrics, University of Florence, Via delle Oblate, 4, 50134 Florence, Italy. E-mail: marcoinzitari{at}gmail.com
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Abstract
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Background. Cognitive decline, particularly when executive functions are compromised, may worsen motor performance (MP) decline in the elderly population. We investigated whether a global test, a memory test, and an attention test predicted MP decline in older community-dwellers with normal baseline MP participating in the Italian Longitudinal Study on Aging (ILSA).
Methods. One thousand fifty-two ILSA participants (71.2 ± 4.8 years old, mean ± standard deviation [SD], 67% men), with normal baseline MP were reassessed after 3 years using the same MP battery. Participants whose MP score reduction from baseline to follow-up was > 75 percentile were considered to be MP decliners. Global cognition, memory, and attention were assessed using the Mini-Mental State Examination (MMSE), the Babcock Story Recall Test (BSRT), and the Digit Cancellation Test (DCT), respectively. The baseline score on each test was examined as a potential predictor of decline in global MP or in single motor tasks.
Results. Baseline scores on the three cognitive tests were worse among the 166 MP decliners, compared with nondecliners. Participants in the lowest quartile of DCT had a > 2-fold higher adjusted risk of declining than did participants in the highest quartile (odds ratio = 2.47, 95% confidence interval, 1.29–4.74). Conversely, MMSE and BSRT scores no longer predicted MP decline after adjustment. Impaired attention strongly predicted the decline in attention-demanding tasks (tandem walking), but also affected routine tasks (walking).
Conclusions. Impairment in a test measuring attention predicts MP decline among older community-dwellers with normal baseline MP. This finding is consistent with the hypothesis that attentional and executive dysfunction is a major determinant of mobility disability in elderly persons.
IMPAIRMENT of either cognitive (1,2) or motor performance (MP) (3,4) is linked with disability in elderly persons. However, the reciprocal and sequential interrelationship between these two impairments in the disabling process is still unclear. Increasing evidence suggests that balance and walking are complex tasks that depend considerably on cognitive control (5). Preserved cognitive functions are thought to be pivotal to correctly plan motor strategies and to control for interferences from the environment (6) and are particularly stressed in challenging situations (7). Deterioration of global cognition (8–10), as well as impairment in executive function-related domains, such as attention, psychomotor speed, and working memory, have been reported to affect MP and to predict falls (11–13). Tasks driven by executive control functions, performed simultaneously with motor tasks, have been shown to alter MP (7,14). Longitudinal studies have mainly focused on abnormal MP as a potential risk factor for, or a preclinical marker of, cognitive decline or dementia (15,16). Very few prospective studies have evaluated the effect of cognitive dysfunctions, particularly in the executive domain, on MP in the general population (1,17–19).
In a previous study examining comorbidities associated with MP decline in a subcohort of elderly community-dwelling participants in the Italian Longitudinal Study on Aging (ILSA), we found that, adjusting for other associated factors, cognitive impairment no dementia (CIND) did not independently predict MP decline (20). Following this observation, we hypothesized that specific cognitive dysfunctions, possibly those affecting the attentional domain, could still be involved with this decline, independent of the diagnosis of CIND, dementia, or other comorbidities associated with MP deterioration in the elderly population. In the present study we investigated, in the same subcohort, impairments in three basic domains—global cognition, memory, and attention—as potential predictors of MP decline.
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METHODS
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Setting
The ILSA, the methodology of which has been detailed elsewhere (21), investigated frequency, determinants, and consequent dysfunctions of age-related cardiovascular and neurological diseases in a population-based cohort of older (
65 years) Italians. A sample of 5632 participants was randomly selected from eight municipalities across Italy. In the screening phase, participants received a structured assessment of their physical and functional status, risk factors, and symptoms and signs suggestive of the diseases under study. In a second phase, specialists from each discipline confirmed the diagnoses through a detailed clinical examination and review of medical records.
Study Sample
We selected 1052 individuals with normal baseline MP (i.e., scoring 14/14 on the MP battery; see below) in 1992, whose MP was reassessed in 1995. Mean age ± standard deviation (SD) was 71 ± 5; 67% were men. Figure 1 illustrates the attrition from the original ILSA sample. As described in a previous article, the higher proportion of men was due to the fact that more women had an already impaired baseline MP (20).
MP Assessment
The ILSA MP battery included six tests that had been previously shown to independently predict falls (22). Tasks and scores were as follows: (i) time to stand from a chair unaided (4 points if 
2, 3 points if > 2 seconds without using the hands; 2 points if 2, 1 point if > 2 seconds using the hands); (ii) number of steps onto a 23-cm step in 10 seconds (2 points if 3; 1 point if < 3 steps); (iii) number of errors during a 2-meter tandem walk along a 5-cm-wide line (2 points if 8; 1 point if > 8 errors); (iv) time the participant could stand on one leg (2 points if 2; 1 point < 2 seconds); (v) 5-meters walking speed at usual pace, starting from a standing position. The average of two trials was considered (2 points if 0.6; 1 point if < 0.6 m/s); (vi) number of steps to complete a 180° turn (2 points if 5; 1 point if > 5 steps). Each task was scored 0 if the participant was unable to perform it. A total score, ranging from 0 (worst MP) to 14 (best MP), was obtained summing up the individual item scores. Two variables were used as outcomes to describe MP decline. First, a binary variable (decliner/nondecliner) was created, reflecting a difference in MP, from baseline to follow-up, above the 75th percentile of the distribution in the study sample, which corresponds to a 2 point difference in the MP total score. Second, the net difference between baseline and follow-up MP scores (
MP) was calculated. For each of the six single tasks, participants were considered decliners if the difference between their baseline and follow-up scores was 1 point.
Cognitive Studies
The whole ILSA sample received a basic cognitive assessment during both the 1992 and 1995 waves. The Mini-Mental State Examination (MMSE) (23) was used to assess global cognition. Episodic memory was assessed using the Babcock Story Recall Test (BSRT) (24), a 21-unit story to be recalled by the participant immediately and after 10 minutes. An event-weighted, hierarchical scoring accounts for the degree of organization of the participant's oral recollection; the immediate and delayed recall tasks and their sum are scored from 0 to 16, worst to best performance. Selective attention was assessed with the Digit Cancellation Test (DCT) (25). As in other cancellation tests, this test has a basic format with three different matrices made up of 13 strings of 10 digits (0–9 in random sequence); each line includes from 0 to 5 targets. Digits have to be crossed out within a time limit (45 seconds/matrix). The score, indicating the number of exact cancellations, ranges from 0 to 60 (worst to best performance). All three tests had been specifically validated for the use in the Italian population.
Participants with an MMSE score < 24 underwent a second level assessment for cognitive impairment with or without dementia, which included the Cambridge Mental Disorders of the Elderly Examination (CAMDEX) B and H, the Pfeffer Functional Activities Questionnaire, the Hamilton Depression Scale, a full neurological examination, and a review of clinical records (2). Final possible diagnoses were: absence of impairment, dementia (Diagnostic and Statistical Manual of Mental Disorders, Third Edition, Revised [DSM-III-R] criteria), or CIND (requiring exclusion of dementia, Cambridge Cognitive Examination for Mental Disorders of the Elderly [CAMCOG] < 80, and clinical judgment based on direct examination, neuropsychological tests, informant interview, Hamilton Depression Scale, and Pfeffer Questionnaire) (2). Depressive symptoms were assessed using the Geriatric Depression Scale (26).
Other Covariates
The following variables, the comprehensive description and operational definition of which can be found elsewhere (20), were included as covariates: age and gender, years of education, marital status, body mass index, the diagnosis of hypertension, as well as the continuous variables systolic and diastolic blood pressure (mmHg), diabetes, total cholesterol (mg/dL), smoking (packs/year), alcohol consumption (g/day), distal symmetric neuropathy, stroke, parkinsonism, angina or myocardial infarction, heart failure, arrhythmias, peripheral artery disease, anemia, bone or joint diseases, global burden of comorbidity (estimated with the number of registered diseases [disease count]), and functional independence (assessed using both the basic activities of daily living [BADL] and the instrumental ADL [IADL]).
Statistical Analyses
Analysis of variance (ANOVA) for continuous variables and the chi-square test for categorical variables were used to test differences in characteristics between decliners and nondecliners. The bivariate association between neuropsychological test scores and MP was analyzed using Pearson correlation (for the outcome MP) and ANOVA (for the outcome decliner vs nondecliner). To test the ability of cognitive performances to predict MP decline, the three test scores were entered separately into two different sets of multivariable models, based on linear regression (outcome: MP) and on logistic regression (outcome: decliner vs nondecliner). In logistic models, cognitive performances were introduced as quartiles of test scores, taking the quartile with the highest score as the reference category. Both linear and logistic regression analyses were first adjusted for age, gender, and education (forced in the model), then for the baseline variables bivariately associated with MP (marital status, CIND, dementia, parkinsonism, distal symmetrical neuropathy, depressive symptoms, heart failure, anemia, number of lost BADL and IADL), as well as for the other two cognitive tests results. Redundant variables were backward deleted (p out =.05) to obtain parsimonious models. Finally, to establish whether a change in attention was associated with a change in follow-up MP, we used ANOVA to compare MP variation across quartiles of DCT difference between baseline and follow-up, adjusting for the same possible confounders previously mentioned. The same analyses were performed after excluding participants with dementia or CIND. Finally, logistic regression was used to test the ability of the cognitive tests, expressed as score quartiles, to predict the decline in individual MP battery subtasks, taking the quartile with the highest score as the reference category and again adjusting for the mentioned possible confounders. A two-sided p value <.05 was considered statistically significant. All analyses were conducted with SPSS 12.0 (Chicago, IL).
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RESULTS
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Based on our definition of decline, 166 (15.8%) of the 1052 participants had declined after 3 years. Compared with participants with preserved MP, decliners were older, more often women, less educated, more often widows, and more likely to have CIND, parkinsonism, distal symmetrical neuropathy, depressive symptoms, heart failure, and anemia, and more likely to need help in BADL and IADL at baseline. Three decliners were already demented at baseline (Table 1).
Decliners had a significantly worse baseline score in all three tests: They scored 26.3 ± 3.6 on the MMSE, 4.4 ± 2.4 on the BSRT, and 38 ± 11.5 on the DCT, compared with 27.5 ± 2.7, 4.8 ± 2.1, and 44.4 ± 10 scored by nondecliners, respectively (all p values <.001). Consistently, each test score was inversely correlated with MP, with r values of –0.149, –0.066, and –0.161, and corresponding p values of <.001,.032, and <.001 for MMSE, BSTR, and DCT, respectively. The risk of MP decline increased progressively with decreasing quartiles of baseline DCT, independent of age, gender, education, marital status, comorbidities (including CIND and dementia), BADL, IADL, and the other two cognitive test scores (Table 2). Compared with participants in the highest quartile, those in the lowest quartile had a > 2-fold greater risk of declining MP. Conversely, the adjusted risk of decline did not change significantly across quartiles of MMSE and BSRT. Both MMSE and DCT predicted MP independent of age, gender, and education, whereas BSRT did not; after further adjustment for confounders (CIND and dementia included), only DCT independently predicted MP (Table 3). All these findings were confirmed after excluding from the study sample the participants with dementia or CIND; DCT maintained a quantitatively similar effect in predicting MP decline (multivariate odds ratio = 2.27, 95% confidence interval, 1.17–4.43, lowest vs highest quartiles of DCT; p for trend across the quartiles =.022). Changes in cognitive performances over time paralleled the MP change: Participants who worsened the most on DCT showed a significantly greater MP reduction (Figure 2).
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Table 2. Effect of Cognitive Status, Expressed as Individual Test Score Quartiles, on the Risk of Motor Performance Decline.
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Figure 2. Mean change in motor performance between baseline and follow-up per quartiles of change in Digit Cancellation Test over time, adjusting for demographics, education, marital status, comorbidities, basic activities of daily living (BADL), and instrumental ADL (IADL) (analysis of variance [ANOVA]). SE = standard error
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When the individual MP tasks were considered (Table 4), the MMSE score was significantly lower among participants who declined in chair standing, step-ups, 180°-turn steps, and one leg standing, compared with participants who did not decline, whereas no difference was observed as a function of walking speed and tandem walking. A lower BSRT was associated with one leg standing decline, whereas the DCT score was significantly lower in participants who declined in all the MP tasks, except for chair standing. After adjusting for demographics and education, MMSE and BSRT no longer independently predicted the decline in MP subtasks. Conversely, participants in the lowest quartile of DCT, compared with those in the highest quartile, had a 2- to 3-fold increased risk of decline in step-ups, walking speed, and 180°-turn steps, even after adjustment for confounders (Table 5). The adjusted risk of decline in tandem walking was > 5-fold higher in participants in the lowest quartile of DCT (Table 5) than in those in the highest quartile.
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Table 4. Differences in Baseline Cognitive Test Scores Between Nondecliners (ND) and Decliners (D) in Motor Performance Test Subtasks (ANOVA).
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Table 5. Independent Predictors of Decline in Motor Performance Battery Subtasks by Quartiles of Digit Cancellation Test (DCT).
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DISCUSSION
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In a population-based cohort of older people with normal baseline MP, a test measuring attention predicted MP decline after 3 years. The longitudinal design of the study and the suggestion of a dose-response trend support the idea that these findings are not confounded by other variables. Conversely, global cognition and memory did not have any independent effect after adjustment for confounders.
Very few population-based studies investigated prospectively the influence of cognitive performance on MP (1,17–19). In the MacArthur Studies of Successful Aging (19), the change in a combined measure of spatial memory, abstract thinking, language, delayed memory, and spatial orientation was independently associated with decline in several physical tasks. In the Hispanic-Established Populations for Epidemiologic Studies of the Elderly (EPESE) (18), the MMSE independently predicted changes in lower extremity performance 2 years later. In contrast with the Hispanic-EPESE (18) and other cross-sectional studies (9,10), in ILSA the effect of global cognition on MP decline largely disappeared when adjusting for confounders. Global cognition predicted physical performance decline in other longitudinal studies, in which, however, only combined, nonselective measures of lower and upper extremity function were used as outcomes (1,17). Notably, in contrast with the MacArthur Study (19), in which a composite measure of cognition was used, in our study the separate evaluation of different cognitive domains suggests a selective involvement of attention deficit in MP decline in elderly persons.
Cross-sectional studies were more detailed in investigating selective cognitive dysfunctions related to MP impairment. In different population-based samples of older persons, tests assessing attention, psychomotor speed, or executive functions (such as the Cancellation Random Figure Test, the Digit Symbol Substitution, the Trail Making Test, or the Stroop test) were independently associated with MP measures (5,11,27). In a recent population-based study, a speed/executive attention factor (which summarized the scores of Trail Making Tests A and B, Block Design, and Digit Symbol Substitution) was associated with a worse gait performance when the attentional demand was maximized using a concurrent verbal task (14).
The hypothesis that some motor tasks are selectively influenced by cognitive impairment was investigated in the MacArthur Study (19). The effect of either baseline cognition or change in cognition between baseline and follow-up was studied separating novel/attentional (one leg standing, tandem standing, tandem walking, foot tapping, walking fast) from routine tasks (chair standing, turning in a circle, normal walking). Changes in cognition were associated with both types of tasks. In our study, DCT predicted the decline in any motor task, specifically, those more attention demanding, such as tandem walking. In more than 900 middle-aged African Americans, worse verbal fluency performance, a task very sensitive to executive abilities, was associated with worse tandem standing and one-leg standing (10). Similar to our findings, in that study chair standing was unrelated to verbal fluency, thus suggesting that motor abilities involved in this test depend more on muscle strength than on cognition.
Strengths of the study include the large, community-based sample, the longitudinal design, and the use of performance-based (rather than self-reported) measures of mobility. Moreover, unlike most previous studies, we considered specific cognitive domains rather than combined measures, and we detailed MP subtasks.
Study limitations are also to be acknowledged. First, there was a large amount of attrition from the original sample, and there was an unbalance between genders. The latter can be explained by greater frailty of women, who were more often already impaired in MP at baseline. Second, only a limited cognitive battery was available; this frequently occurs in secondary analyses of large population-based studies on aging issues like ILSA. However, the three tests we used are universally considered to be valid to assess related domains functions, and have been specifically validated for their application to the Italian population.
Summary
Impaired performance in a test assessing attention, not in measures of global cognition or memory, predicted MP decline in older community-dwellers with initially preserved mobility. Our observations are concordant with the increasing evidence suggesting that walking is under cognitive control, with executive domain functions playing a relevant role (5). In our study, impaired attention had the greatest impact on attention-demanding motor tasks, but it also affected measures of routine tasks, such as walking speed. Reduced walking speed has been shown to independently predict hospitalization, institutionalization, falls, fractures, and death in older adults (28).
From the clinical practice viewpoint, DCT, a simple, objective, and validated test for attention, might be proposed as a routine tool for the prediction of motor decline in older persons. Further prospective studies, possibly using larger cognitive test batteries to describe more selectively single domain impairments, will be welcome to corroborate these initial observations.
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Acknowledgments
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The ILSA was supported by the Italian National Research Council (Targeted Project "Aging," 1991–1998). Since 1999 it has been supported by the Italian National Research Council (Project "Biology of Aging") and by the Italian Health Ministry (Program "Epidemiology of the Elderly" of the Istituto Superiore di Sanità and Special Program "Estimates of Health Needs of the Elderly" of the Tuscany Region).
We thank M.E. Della Santa who contributed to the manuscript preparation.
The ILSA Working Group: A. Di Carlo, MD, M. Baldereschi, MD, S. Maggi, MD, Italian National Research Council, Italy; G. Scarlato, MD, L. Candelise, MD, E. Scarpini, MD, University of Milano, Italy; P. Carbonin, MD, Università Cattolica del Sacro Cuore, Roma, Italy; G. Farchi, MSc, E. Scafato, MD, Istituto Superiore di Sanità, Roma, Italy; F. Grigoletto, ScD, E. Perissinotto, ScD, L. Battistin, MD, M. Bressan, MD, G. Enzi, MD, G. Bortolan, ScD, University of Padova, Italy; C. Loeb, MD, Italian National Research Council, Genova, Italy; C. Gandolfo, MD, University of Genova, Italy; N. Canal, MD, M. Franceschi, MD, San Raffaele Institute, Milano, Italy; A. Ghetti, MD, R. Vergassola, MD, Health Area 10, Firenze, Italy; L. Amaducci, MD, D. Inzitari, MD, University of Firenze, Italy; S. Bonaiuto, MD, F. Fini, MD, A. Vesprini, MD, G. Cruciani, MD, INRCA Fermo, Italy; A. Capurso, MD, P. Livrea, MD, V. Lepore, MD, University of Bari, Italy; L. Motta, MD, G. Carnazzo, MD, P. Bentivegna, University of Catania, Italy; F. Rengo, MD, University of Napoli, Italy.
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Footnotes
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Decision Editor: Luigi Ferrucci, MD, PhD
Received July 19, 2006
Accepted October 16, 2006
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Abstract
Methods
